Epigenomic effects of vitamin D in colorectal cancer

Papers of special note have been highlighted as: • of interest; •• of considerable interest

References

• 1. Bikle DD. Vitamin D metabolism, mechanism of action, and clinical applications. Chem. Biol. 21(3), 319–329 (2014). • A comprehensive review on the metabolism of vitamin D and its mechanism of action.
  Medline CASGoogle Scholar
• 2. Goltzman D. Functions of vitamin D in bone. Histochem. Cell Biol. 149(4), 305–312 (2018).
  Medline CASGoogle Scholar
• 3. Keum N, Lee DH, Greenwood DC, Manson JE, Giovannucci E. Vitamin D supplementation and total cancer incidence and mortality: a meta-analysis of randomized controlled trials. Ann. Oncol. 30(5), 733–743 (2019). •• An updated meta-analysis of randomized clinical trials that focuses on the effect of vitamin D supplementation on cancer mortality and incidence in more than 6000 samples.
  Medline CASGoogle Scholar
• 4. Zhang Y, Fang F, Tang J et al. Association between vitamin D supplementation and mortality: systematic review and meta-analysis. BMJ 366, l4673 (2019).
  MedlineGoogle Scholar
• 5. Chandler PD, Chen WY, Ajala ON et al. Effect of vitamin D3 supplements on development of advanced cancer: a secondary analysis of the VITAL randomized clinical trial. JAMA Netw. Open 3(11), e2025850 (2020). •• Clinical trial on more than 25,000 patients with cancer evaluating the effect of vitamin D supplementation.
  MedlineGoogle Scholar
• 6. Feldman D, Krishnan AV, Swami S, Giovannucci E, Feldman BJ. The role of vitamin D in reducing cancer risk and progression. Nat. Rev. Cancer 14(5), 342–357 (2014).
  Medline CASGoogle Scholar
• 7. Dou R, Ng K, Giovannucci EL, Manson JE, Qian ZR, Ogino S. Vitamin D and colorectal cancer: molecular, epidemiological and clinical evidence. Br. J. Nutr. 115(9), 1643–1660 (2016).
  Medline CASGoogle Scholar
• 8. Janakiram NB, Mohammed A, Madka V, Kumar G, Rao CV. Prevention and treatment of cancers by immune modulating nutrients. Mol. Nutr. Food Res. 60(6), 1275–1294 (2016).
  Medline CASGoogle Scholar
• 9. Van Harten-Gerritsen AS, Balvers MG, Witkamp RF, Kampman E, Van Duijnhoven FJ. Vitamin D, inflammation, and colorectal cancer progression: a review of mechanistic studies and future directions for epidemiological studies. Cancer Epidemiol. Biomarkers Prev. 24(12), 1820–1828 (2015).
  Medline CASGoogle Scholar
• 10. Veldhoen M, Brucklacher-Waldert V. Dietary influences on intestinal immunity. Nat. Rev. Immunol. 12(10), 696–708 (2012).
  Medline CASGoogle Scholar
• 11. Von Essen MR, Kongsbak M, Schjerling P, Olgaard K, Odum N, Geisler C. Vitamin D controls T cell antigen receptor signaling and activation of human T cells. Nat. Immunol. 11(4), 344–349 (2010).
  Medline CASGoogle Scholar
• 12. Song M, Nishihara R, Wang M et al. Plasma 25-hydroxyvitamin D and colorectal cancer risk according to tumour immunity status. Gut 65(2), 296–304 (2016).
  Medline CASGoogle Scholar
• 13. Meeker S, Seamons A, Paik J et al. Increased dietary vitamin D suppresses MAPK signaling, colitis, and colon cancer. Cancer Res. 74(16), 4398–4408 (2014).
  Medline CASGoogle Scholar
• 14. Almouazen E, Bourgeois S, Jordheim LP, Fessi H, Briançon S. Nano-encapsulation of vitamin D3 active metabolites for application in chemotherapy: formulation study and in vitro evaluation. Pharm. Res. 30(4), 1137–1146 (2013).
  Medline CASGoogle Scholar
• 15. Glowka E, Stasiak J, Lulek J. Drug delivery systems for vitamin D supplementation and therapy. Pharmaceutics 11(7), 347 (2019).
  CASGoogle Scholar
• 16. Jain KK. Current status and future prospects of drug delivery systems. Methods Mol. Biol. 1141, 1–56 (2014).
  Medline CASGoogle Scholar
• 17. Banik BL, Fattahi P, Brown JL. Polymeric nanoparticles: the future of nanomedicine. Wiley Interdiscip. Rev. Nanomed. Nanobiotechnol. 8(2), 271–299 (2016).
  MedlineGoogle Scholar
• 18. Duffy MJ, Murray A, Synnott NC, O'donovan N, Crown J. Vitamin D analogues: potential use in cancer treatment. Crit. Rev. Oncol. Hematol. 112, 190–197 (2017).
  MedlineGoogle Scholar
• 19. Siegel RL, Miller KD, Goding Sauer A et al. Colorectal cancer statistics, 2020. CA Cancer J. Clin. 70(3), 145–164 (2020).
  MedlineGoogle Scholar
• 20. Dekker E, Tanis PJ, Vleugels JLA, Kasi PM, Wallace MB. Colorectal cancer. Lancet 394(10207), 1467–1480 (2019). •• A great review summarizing colorectal cancer etiology, diagnosis, and treatment status.
  MedlineGoogle Scholar
• 21. Wassenaar TM. E. coli and colorectal cancer: a complex relationship that deserves a critical mindset. Crit. Rev. Microbiol. 44(5), 619–632 (2018).
  MedlineGoogle Scholar
• 22. Wong SH, Yu J. Gut microbiota in colorectal cancer: mechanisms of action and clinical applications. Nat. Rev. Gastroenterol. Hepatol. 16(11), 690–704 (2019). • Focuses on clinical applications of gut microbiota in screening, prognosis, prediction and prevention of cancer.
  Medline CASGoogle Scholar
• 23. Hessami Arani S, Kerachian MA. Rising rates of colorectal cancer among younger Iranians: is diet to blame? Curr. Oncol. 24(2), e131–e137 (2017).
  MedlineGoogle Scholar
• 24. Gandini S, Boniol M, Haukka J et al. Meta-analysis of observational studies of serum 25-hydroxyvitamin D levels and colorectal, breast and prostate cancer and colorectal adenoma. Int. J. Cancer 128(6), 1414–1424 (2011).
  Medline CASGoogle Scholar
• 25. Lee JE, Li H, Chan AT et al. Circulating levels of vitamin D and colon and rectal cancer: the Physicians' Health Study and a meta-analysis of prospective studies. Cancer Prev. Res. (Phila.) 4(5), 735–743 (2011).
  Medline CASGoogle Scholar
• 26. Ma Y, Zhang P, Wang F, Yang J, Liu Z, Qin H. Association between vitamin D and risk of colorectal cancer: a systematic review of prospective studies. J. Clin. Oncol. 29(28), 3775–3782 (2011).
  Medline CASGoogle Scholar
• 27. Touvier M, Chan DS, Lau R et al. Meta-analyses of vitamin D intake, 25-hydroxyvitamin D status, vitamin D receptor polymorphisms, and colorectal cancer risk. Cancer Epidemiol. Biomarkers Prev. 20(5), 1003–1016 (2011).
  Medline CASGoogle Scholar
• 28. Garland CF, Garland FC. Do sunlight and vitamin D reduce the likelihood of colon cancer? Int. J. Epidemiol. 9(3), 227–231 (1980).
  Medline CASGoogle Scholar
• 29. Garland CF, Comstock GW, Garland FC, Helsing KJ, Shaw EK, Gorham ED. Serum 25-hydroxyvitamin D and colon cancer: eight-year prospective study. Lancet 2(8673), 1176–1178 (1989).
  Medline CASGoogle Scholar
• 30. Song M, Garrett WS, Chan AT. Nutrients, foods, and colorectal cancer prevention. Gastroenterology 148(6), 1244–1260.e1216 (2015).
  Medline CASGoogle Scholar
• 31. Ng K, Sargent DJ, Goldberg RM et al. Vitamin D status in patients with stage IV colorectal cancer: findings from Intergroup trial N9741. J. Clin. Oncol. 29(12), 1599–1606 (2011).
  Medline CASGoogle Scholar
• 32. McCullough ML, Zoltick ES, Weinstein SJ et al. Circulating vitamin D and colorectal cancer risk: an international pooling project of 17 cohorts. J. Natl Cancer Inst. 111(2), 158–169 (2019).
  MedlineGoogle Scholar
• 33. Urashima M, Ohdaira H, Akutsu T et al. Effect of vitamin D supplementation on relapse-free survival among patients with digestive tract cancers: the AMATERASU randomized clinical trial. JAMA 321(14), 1361–1369 (2019).
  Medline CASGoogle Scholar
• 34. Ng K, Nimeiri HS, Mccleary NJ et al. Effect of high-dose vs standard-dose vitamin D3 supplementation on progression-free survival among patients with advanced or metastatic colorectal cancer: the SUNSHINE randomized clinical trial. JAMA 321(14), 1370–1379 (2019).
  Medline CASGoogle Scholar
• 35. Lappe JM, Travers-Gustafson D, Davies KM, Recker RR, Heaney RP. Vitamin D and calcium supplementation reduces cancer risk: results of a randomized trial. Am. J. Clin. Nutr. 85(6), 1586–1591 (2007).
  Medline CASGoogle Scholar
• 36. Klutstein M, Nejman D, Greenfield R, Cedar H. DNA methylation in cancer and aging. Cancer Res. 76(12), 3446–3450 (2016).
  Medline CASGoogle Scholar
• 37. Mahmood N, Rabbani SA. DNA methylation readers and cancer: mechanistic and therapeutic applications. Front. Oncol. 9, 489 (2019).
  MedlineGoogle Scholar
• 38. Chatterjee A, Rodger EJ, Eccles MR. Epigenetic drivers of tumourigenesis and cancer metastasis. Semin. Cancer Biol. 51, 149–159 (2018).
  Medline CASGoogle Scholar
• 39. Chik F, Szyf M, Rabbani SA. Role of epigenetics in cancer initiation and progression. Adv. Exp. Med. Biol. 720, 91–104 (2011).
  Medline CASGoogle Scholar
• 40. Jones PA, Baylin SB. The fundamental role of epigenetic events in cancer. Nat. Rev. Genet. 3(6), 415–428 (2002).
  Medline CASGoogle Scholar
• 41. Patil V, Ward RL, Hesson LB. The evidence for functional non-CpG methylation in mammalian cells. Epigenetics 9(6), 823–828 (2014).
  MedlineGoogle Scholar
• 42. Bhattacharya SK, Ramchandani S, Cervoni N, Szyf M. A mammalian protein with specific demethylase activity for mCpG DNA. Nature 397(6720), 579–583 (1999).
  Medline CASGoogle Scholar
• 43. Cheishvili D, Chik F, Li CC et al. Synergistic effects of combined DNA methyltransferase inhibition and MBD2 depletion on breast cancer cells; MBD2 depletion blocks 5-aza-2′-deoxycytidine-triggered invasiveness. Carcinogenesis 35(11), 2436–2446 (2014).
  Medline CASGoogle Scholar
• 44. Hendrich B, Bird A. Identification and characterization of a family of mammalian methyl-CpG binding proteins. Mol. Cell. Biol. 18(11), 6538–6547 (1998).
  Medline CASGoogle Scholar
• 45. Ehrlich M. DNA hypomethylation in cancer cells. Epigenomics 1(2), 239–259 (2009).
  CASGoogle Scholar
• 46. Robertson KD. DNA methylation and human disease. Nat. Rev. Genet. 6(8), 597–610 (2005).
  Medline CASGoogle Scholar
• 47. Cavalli G, Heard E. Advances in epigenetics link genetics to the environment and disease. Nature 571(7766), 489–499 (2019).
  Medline CASGoogle Scholar
• 48. Chen Q, Zhu C, Jin Y. The oncogenic and tumor suppressive functions of the long noncoding RNA MALAT1: an emerging controversy. Front. Genet. 11, 93 (2020).
  Medline CASGoogle Scholar
• 49. Poursheikhani A, Abbaszadegan MR, Kerachian MA. Mechanisms of long non-coding RNA function in colorectal cancer tumorigenesis. Asia Pac. J. Clin. Oncol. 17(1), 7–23 (2021).
  MedlineGoogle Scholar
• 50. Yang X, Liu M, Li M et al. Epigenetic modulations of noncoding RNA: a novel dimension of cancer biology. Mol. Cancer 19(1), 64 (2020).
  MedlineGoogle Scholar
• 51. Yao Q, Chen Y, Zhou X. The roles of microRNAs in epigenetic regulation. Curr. Opin. Chem. Biol. 51, 11–17 (2019).
  Medline CASGoogle Scholar
• 52. Gillette TG, Hill JA. Readers, writers, and erasers. Circ. Res. 116(7), 1245–1253 (2015).
  Medline CASGoogle Scholar
• 53. Schuettengruber B, Bourbon HM, Di Croce L, Cavalli G. Genome regulation by polycomb and trithorax: 70 years and counting. Cell 171(1), 34–57 (2017).
  Medline CASGoogle Scholar
• 54. McDonald OG, Li X, Saunders T et al. Epigenomic reprogramming during pancreatic cancer progression links anabolic glucose metabolism to distant metastasis. Nat. Genet. 49(3), 367–376 (2017).
  Medline CASGoogle Scholar
• 55. Ropero S, Esteller M. The role of histone deacetylases (HDACs) in human cancer. Mol. Oncol. 1(1), 19–25 (2007).
  Medline CASGoogle Scholar
• 56. Morera L, Lübbert M, Jung M. Targeting histone methyltransferases and demethylases in clinical trials for cancer therapy. Clin. Epigenetics 8(1), 57 (2016).
  MedlineGoogle Scholar
• 57. Fang Y, Liao G, Yu B. LSD1/KDM1A inhibitors in clinical trials: advances and prospects. J. Hematol. Oncol. 12(1), 129 (2019).
  MedlineGoogle Scholar
• 58. Herman JG, Umar A, Polyak K et al. Incidence and functional consequences of hMLH1 promoter hypermethylation in colorectal carcinoma. Proc. Natl Acad. Sci. U. S. A. 95(12), 6870–6875 (1998).
  Medline CASGoogle Scholar
• 59. Jung G, Hernández-Illán E, Moreira L, Balaguer F, Goel A. Epigenetics of colorectal cancer: biomarker and therapeutic potential. Nat. Rev. Gastroenterol. Hepatol. 17(2), 111–130 (2020).
  MedlineGoogle Scholar
• 60. Hur K, Cejas P, Feliu J et al. Hypomethylation of long interspersed nuclear element-1 (LINE-1) leads to activation of proto-oncogenes in human colorectal cancer metastasis. Gut 63(4), 635–646 (2014).
  Medline CASGoogle Scholar
• 61. Milicic A, Harrison LA, Goodlad RA et al. Ectopic expression of P-cadherin correlates with promoter hypomethylation early in colorectal carcinogenesis and enhanced intestinal crypt fission in vivo. Cancer Res. 68(19), 7760–7768 (2008).
  Medline CASGoogle Scholar
• 62. Nagai Y, Sunami E, Yamamoto Y et al. LINE-1 hypomethylation status of circulating cell-free DNA in plasma as a biomarker for colorectal cancer. Oncotarget 8(7), 11906–11916 (2017).
  MedlineGoogle Scholar
• 63. Pérez RF, Tejedor JR, Bayón GF, Fernández AF, Fraga MF. Distinct chromatin signatures of DNA hypomethylation in aging and cancer. Aging Cell 17(3), e12744 (2018).
  MedlineGoogle Scholar
• 64. Sunami E, De Maat M, Vu A, Turner RR, Hoon DS. LINE-1 hypomethylation during primary colon cancer progression. PLOS ONE 6(4), e18884 (2011).
  Medline CASGoogle Scholar
• 65. Luo J, Li YN, Wang F, Zhang WM, Geng X. S-adenosylmethionine inhibits the growth of cancer cells by reversing the hypomethylation status of c-myc and H-ras in human gastric cancer and colon cancer. Int. J. Biol. Sci. 6(7), 784–795 (2010).
  Medline CASGoogle Scholar
• 66. Antelo M, Balaguer F, Shia J et al. A high degree of LINE-1 hypomethylation is a unique feature of early-onset colorectal cancer. PLOS ONE 7(9), e45357 (2012).
  Medline CASGoogle Scholar
• 67. Baba Y, Yagi T, Sawayama H et al. Long interspersed element-1 methylation level as a prognostic biomarker in gastrointestinal cancers. Digestion 97(1), 26–30 (2018).
  Medline CASGoogle Scholar
• 68. Castellano-Castillo D, Morcillo S, Crujeiras AB et al. Association between serum 25-hydroxyvitamin D and global DNA methylation in visceral adipose tissue from colorectal cancer patients. BMC Cancer 19(1), 93 (2019).
  MedlineGoogle Scholar
• 69. McVeigh G, Galloway D, Johnston D. The case for low dose diuretics in hypertension: comparison of low and conventional doses of cyclopenthiazide. BMJ 297(6641), 95–98 (1988).
  Medline CASGoogle Scholar
• 70. Kerachian MA, Kerachian M. Long interspersed nucleotide element-1 (LINE-1) methylation in colorectal cancer. Clin. Chim. Acta 488, 209–214 (2019).
  Medline CASGoogle Scholar
• 71. Ogino S, Kawasaki T, Nosho K et al. LINE-1 hypomethylation is inversely associated with microsatellite instability and CpG island methylator phenotype in colorectal cancer. Int. J. Cancer 122(12), 2767–2773 (2008).
  Medline CASGoogle Scholar
• 72. Suter CM, Martin DI, Ward RL. Hypomethylation of L1 retrotransposons in colorectal cancer and adjacent normal tissue. Int. J. Colorectal Dis. 19(2), 95–101 (2004).
  MedlineGoogle Scholar
• 73. Ma Y, Zhang P, Yang J, Liu Z, Yang Z, Qin H. Candidate microRNA biomarkers in human colorectal cancer: systematic review profiling studies and experimental validation. Int. J. Cancer 130(9), 2077–2087 (2012).
  Medline CASGoogle Scholar
• 74. Strubberg AM, Madison BB. MicroRNAs in the etiology of colorectal cancer: pathways and clinical implications. Dis. Model. Mech. 10(3), 197–214 (2017).
  Medline CASGoogle Scholar
• 75. Svoronos AA, Engelman DM, Slack FJ. OncomiR or tumor suppressor? The duplicity of microRNAs in cancer. Cancer Res. 76(13), 3666–3670 (2016).
  Medline CASGoogle Scholar
• 76. Chen X, Guo X, Zhang H et al. Role of miR-143 targeting KRAS in colorectal tumorigenesis. Oncogene 28(10), 1385–1392 (2009).
  Medline CASGoogle Scholar
• 77. Horiuchi A, Iinuma H, Akahane T, Shimada R, Watanabe T. Prognostic significance of PDCD4 expression and association with microRNA-21 in each Dukes' stage of colorectal cancer patients. Oncol. Rep. 27(5), 1384–1392 (2012).
  Medline CASGoogle Scholar
• 78. Peacock O, Lee AC, Cameron F et al. Inflammation and MiR-21 pathways functionally interact to downregulate PDCD4 in colorectal cancer. PLOS ONE 9(10), e110267 (2014).
  MedlineGoogle Scholar
• 79. Wu Y, Song Y, Xiong Y et al. MicroRNA-21 (Mir-21) promotes cell growth and invasion by repressing tumor suppressor PTEN in colorectal cancer. Cell. Physiol. Biochem. 43(3), 945–958 (2017).
  Medline CASGoogle Scholar
• 80. Luo ZF, Zhao D, Li XQ et al. Clinical significance of HOTAIR expression in colon cancer. World J. Gastroenterol. 22(22), 5254–5259 (2016).
  Medline CASGoogle Scholar
• 81. Schwarzenbach H. Biological and clinical relevance of H19 in colorectal cancer patients. EBioMedicine 13, 9–10 (2016).
  MedlineGoogle Scholar
• 82. Audia JE, Campbell RM. Histone modifications and cancer. Cold Spring Harb. Perspect. Biol. 8(4), a019521 (2016).
  MedlineGoogle Scholar
• 83. Vaish V, Khare T, Verma M, Khare S. Epigenetic therapy for colorectal cancer. Methods Mol. Biol. 1238, 771–782 (2015).
  MedlineGoogle Scholar
• 84. Huang T, Lin C, Zhong LL et al. Targeting histone methylation for colorectal cancer. Therap. Adv. Gastroenterol. 10(1), 114–131 (2017).
  Medline CASGoogle Scholar
• 85. Salz T, Li G, Kaye F, Zhou L, Qiu Y, Huang S. hSETD1A regulates Wnt target genes and controls tumor growth of colorectal cancer cells. Cancer Res. 74(3), 775–786 (2014).
  Medline CASGoogle Scholar
• 86. Mahmood N, Rabbani SA. DNA methylation readers and cancer: mechanistic and therapeutic applications. Front. Oncol. 9, 489 (2019).
  MedlineGoogle Scholar
• 87. Quintero E, Castells A, Bujanda L et al. Colonoscopy versus fecal immunochemical testing in colorectal-cancer screening. N. Engl. J. Med. 366(8), 697–706 (2012).
  Medline CASGoogle Scholar
• 88. Kormi SMA, Ardehkhani S, Kerachian MA. New insights into colorectal cancer screening and early detection tests. Colorectal Cancer 6(2), 63–68 (2017).
  Google Scholar
• 89. Devos T, Tetzner R, Model F et al. Circulating methylated SEPT9 DNA in plasma is a biomarker for colorectal cancer. Clin. Chem. 55(7), 1337–1346 (2009).
  Medline CASGoogle Scholar
• 90. Jamialahmadi K, Azghandi M, Javadmanesh A, Zardadi M, Shams Davodly E, Kerachian MA. A DNA methylation panel for high performance detection of colorectal cancer. Cancer Genet. 252–253, 64–72 (2021).
  Medline CASGoogle Scholar
• 91. Yang Q, Huang T, Ye G, Wang B, Zhang X. Methylation of SFRP2 gene as a promising noninvasive biomarker using feces in colorectal cancer diagnosis: a systematic meta-analysis. Sci. Rep. 6, 33339 (2016).
  Medline CASGoogle Scholar
• 92. Boughanem H, Cabrera-Mulero A, Hernández-Alonso P et al. Association between variation of circulating 25-OH vitamin D and methylation of secreted frizzled-related protein 2 in colorectal cancer. Clin. Epigenetics 12(1), 83 (2020).
  Medline CASGoogle Scholar
• 93. Tapp HS, Commane DM, Bradburn DM et al. Nutritional factors and gender influence age-related DNA methylation in the human rectal mucosa. Aging Cell 12(1), 148–155 (2013).
  Medline CASGoogle Scholar
• 94. Rawson JB, Sun Z, Dicks E et al. Vitamin D intake is negatively associated with promoter methylation of the Wnt antagonist gene DKK1 in a large group of colorectal cancer patients. Nutr. Cancer 64(7), 919–928 (2012).
  Medline CASGoogle Scholar
• 95. Yang R, Zhang J, Li J et al. Inhibition of Nrf2 degradation alleviates age-related osteoporosis induced by 1,25-Dihydroxyvitamin D deficiency. Free Radic. Biol. Med. 178, 246–261 (2022).
  Medline CASGoogle Scholar
• 96. Gregoretti I, Lee Y-M, Goodson HV. Molecular evolution of the histone deacetylase family: functional implications of phylogenetic analysis. J. Mol. Biol. 338(1), 17–31 (2004).
  Medline CASGoogle Scholar
• 97. Sun M, Guo B. Vitamin D and the epigenetic machinery in colon cancer. Curr. Med. Chem. 24(9), 888–897 (2017).
  Medline CASGoogle Scholar
• 98. Godman CA, Joshi R, Tierney BR et al. HDAC3 impacts multiple oncogenic pathways in colon cancer cells with effects on Wnt and vitamin D signaling. Cancer Biol. Ther. 7(10), 1570–1580 (2008).
  Medline CASGoogle Scholar
• 99. Hossain S, Liu Z, Wood RJ. Association between histone deacetylase activity and vitamin D-dependent gene expressions in relation to sulforaphane in human colorectal cancer cells. J. Sci. Food Agric. 101(5), 1833–1843 (2021).
  Medline CASGoogle Scholar
• 100. Pereira F, Barbáchano A, Silva J et al. KDM6B/JMJD3 histone demethylase is induced by vitamin D and modulates its effects in colon cancer cells. Hum. Mol. Genet. 20(23), 4655–4665 (2011).
  Medline CASGoogle Scholar
• 101. Lan F, Bayliss PE, Rinn JL et al. A histone H3 lysine 27 demethylase regulates animal posterior development. Nature 449(7163), 689–694 (2007).
  Medline CASGoogle Scholar
• 102. De Santa F, Totaro MG, Prosperini E, Notarbartolo S, Testa G, Natoli G. The histone H3 lysine-27 demethylase Jmjd3 links inflammation to inhibition of polycomb-mediated gene silencing. Cell 130(6), 1083–1094 (2007).
  MedlineGoogle Scholar
• 103. Hong S, Cho YW, Yu LR, Yu H, Veenstra TD, Ge K. Identification of JmjC domain-containing UTX and JMJD3 as histone H3 lysine 27 demethylases. Proc. Natl Acad. Sci. USA 104(47), 18439–18444 (2007).
  Medline CASGoogle Scholar
• 104. Agger K, Cloos PA, Christensen J et al. UTX and JMJD3 are histone H3K27 demethylases involved in HOX gene regulation and development. Nature 449(7163), 731–734 (2007).
  Medline CASGoogle Scholar
• 105. Pereira F, Barbáchano A, Singh PK, Campbell MJ, Muñoz A, Larriba MJ. Vitamin D has wide regulatory effects on histone demethylase genes. Cell Cycle 11(6), 1081–1089 (2012).
  Medline CASGoogle Scholar
• 106. Padi SK, Zhang Q, Rustum YM, Morrison C, Guo B. MicroRNA-627 mediates the epigenetic mechanisms of vitamin D to suppress proliferation of human colorectal cancer cells and growth of xenograft tumors in mice. Gastroenterology 145(2), 437–446 (2013).
  Medline CASGoogle Scholar
• 107. Kasiappan R, Shen Z, Tse AK et al. 1,25-Dihydroxyvitamin D3 suppresses telomerase expression and human cancer growth through microRNA-498. J. Biol. Chem. 287(49), 41297–41309 (2012).
  Medline CASGoogle Scholar
• 108. Komagata S, Nakajima M, Takagi S, Mohri T, Taniya T, Yokoi T. Human CYP24 catalyzing the inactivation of calcitriol is post-transcriptionally regulated by miR-125b. Mol. Pharmacol. 76(4), 702–709 (2009).
  Medline CASGoogle Scholar
• 109. Ting HJ, Messing J, Yasmin-Karim S, Lee YF. Identification of microRNA-98 as a therapeutic target inhibiting prostate cancer growth and a biomarker induced by vitamin D. J. Biol. Chem. 288(1), 1–9 (2013).
  Medline CASGoogle Scholar
• 110. Mohri T, Nakajima M, Takagi S, Komagata S, Yokoi T. MicroRNA regulates human vitamin D receptor. Int. J. Cancer 125(6), 1328–1333 (2009).
  Medline CASGoogle Scholar
• 111. Gocek E, Wang X, Liu X, Liu CG, Studzinski GP. MicroRNA-32 upregulation by 1,25-dihydroxyvitamin D3 in human myeloid leukemia cells leads to Bim targeting and inhibition of AraC-induced apoptosis. Cancer Res. 71(19), 6230–6239 (2011).
  Medline CASGoogle Scholar
• 112. Wang X, Gocek E, Liu CG, Studzinski GP. MicroRNAs181 regulate the expression of p27Kip1 in human myeloid leukemia cells induced to differentiate by 1,25-dihydroxyvitamin D3. Cell Cycle 8(5), 736–741 (2009).
  Medline CASGoogle Scholar
• 113. Giangreco AA, Vaishnav A, Wagner D et al. Tumor suppressor microRNAs, miR-100 and -125b, are regulated by 1,25-dihydroxyvitamin D in primary prostate cells and in patient tissue. Cancer Prev. Res. (Phila.) 6(5), 483–494 (2013).
  Medline CASGoogle Scholar
• 114. Negri M, Gentile A, De Angelis C et al. Vitamin D-induced molecular mechanisms to potentiate cancer therapy and to reverse drug-resistance in cancer cells. Nutrients 12(6), 1798 (2020).
  CASGoogle Scholar
• 115. Wang J, Li Y, Ding M, Zhang H, Xu X, Tang J. Molecular mechanisms and clinical applications of miR-22 in regulating malignant progression in human cancer (review). Int. J. Oncol. 50(2), 345–355 (2017).
  Medline CASGoogle Scholar
• 116. Alvarez-Díaz S, Valle N, Ferrer-Mayorga G et al. MicroRNA-22 is induced by vitamin D and contributes to its antiproliferative, antimigratory and gene regulatory effects in colon cancer cells. Hum. Mol. Genet. 21(10), 2157–2165 (2012).
  Medline CASGoogle Scholar
• 117. Sun M, Zhang Q, Yang X, Qian SY, Guo B. Vitamin D enhances the efficacy of irinotecan through miR-627-mediated inhibition of intratumoral drug metabolism. Mol. Cancer Ther. 15(9), 2086–2095 (2016).
  Medline CASGoogle Scholar
• 118. Lin W, Zou H, Mo J et al. Micro1278 leads to tumor growth arrest, enhanced sensitivity to oxaliplatin and vitamin D and inhibits metastasis via KIF5B, CYP24A1, and BTG2, respectively. Front. Oncol. 11, 637878 (2021).
  MedlineGoogle Scholar
• 119. Essa S, Denzer N, Mahlknecht U et al. VDR microRNA expression and epigenetic silencing of vitamin D signaling in melanoma cells. J. Steroid Biochem. Mol. Biol. 121(1–2), 110–113 (2010).
  Medline CASGoogle Scholar
• 120. Pan YZ, Gao W, Yu AM. MicroRNAs regulate CYP3A4 expression via direct and indirect targeting. Drug Metab. Dispos. 37(10), 2112–2117 (2009).
  Medline CASGoogle Scholar
• 121. Essa S, Reichrath S, Mahlknecht U et al. Signature of VDR miRNAs and epigenetic modulation of vitamin D signaling in melanoma cell lines. Anticancer Res. 32(1), 383–389 (2012).
  Medline CASGoogle Scholar
• 122. Wang W, Xie Y, Chen F et al. LncRNA MEG3 acts a biomarker and regulates cell functions by targeting ADAR1 in colorectal cancer. World J. Gastroenterol. 25(29), 3972–3984 (2019).
  Medline CASGoogle Scholar
• 123. Zhu Y, Chen P, Gao Y et al. MEG3 activated by vitamin D inhibits colorectal cancer cells proliferation and migration via regulating clusterin. EBioMedicine 30, 148–157 (2018).
  MedlineGoogle Scholar
• 124. Zuo S, Wu L, Wang Y, Yuan X. Long non-coding RNA MEG3 activated by vitamin D suppresses glycolysis in colorectal cancer via promoting c-Myc degradation. Front. Oncol. 10, 274 (2020).
  MedlineGoogle Scholar
• 125. Wu X, Li J, Ren Y, Zuo Z, Ni S, Cai J. MEG3 can affect the proliferation and migration of colorectal cancer cells through regulating miR-376/PRKD1 axis. Am. J. Transl. Res. 11(9), 5740–5751 (2019).
  Medline CASGoogle Scholar
• 126. Chen S, Bu D, Ma Y et al. H19 overexpression induces resistance to 1,25(OH)2D3 by rargeting VDR through miR-675-5p in colon cancer cells. Neoplasia 19(3), 226–236 (2017).
  Medline CASGoogle Scholar
• 127. Anderson MG, Nakane M, Ruan X, Kroeger PE, Wu-Wong JR. Expression of VDR and CYP24A1 mRNA in human tumors. Cancer Chemother. Pharmacol. 57(2), 234–240 (2006).
  Medline CASGoogle Scholar
• 128. Bareis P, Bises G, Bischof MG, Cross HS, Peterlik M. 25-hydroxy-vitamin d metabolism in human colon cancer cells during tumor progression. Biochem. Biophys. Res. Commun. 285(4), 1012–1017 (2001).
  Medline CASGoogle Scholar
• 129. Luo W, Karpf AR, Deeb KK et al. Epigenetic regulation of vitamin D 24-hydroxylase/CYP24A1 in human prostate cancer. Cancer Res. 70(14), 5953–5962 (2010).
  Medline CASGoogle Scholar
• 130. Chung I, Karpf AR, Muindi JR et al. Epigenetic silencing of CYP24 in tumor-derived endothelial cells contributes to selective growth inhibition by calcitriol. J. Biol. Chem. 282(12), 8704–8714 (2007).
  Medline CASGoogle Scholar
• 131. Kósa JP, Horváth P, Wölfling J et al. CYP24A1 inhibition facilitates the anti-tumor effect of vitamin D3 on colorectal cancer cells. World J. Gastroenterol. 19(17), 2621–2628 (2013).
  Medline CASGoogle Scholar
• 132. Sun H, Jiang C, Cong L et al. CYP24A1 inhibition facilitates the antiproliferative effect of 1,25(OH)(2)D(3) through downregulation of the WNT/β-catenin pathway and methylation-mediated regulation of CYP24A1 in Colorectal cancer cells. DNA Cell Biol. 37(9), 742–749 (2018).
  Medline CASGoogle Scholar
• 133. Mahmood N, Arakelian A, Muller WJ, Szyf M, Rabbani SA. An enhanced chemopreventive effect of methyl donor S-adenosylmethionine in combination with 25-hydroxyvitamin D in blocking mammary tumor growth and metastasis. Bone Res. 8, 28 (2020). • Provides a novel strategy to reduce breast cancer-associated morbidity and mortality using vitamin D.
  Medline CASGoogle Scholar
• 134. Hu PS, Li T, Lin JF et al. VDR-SOX2 signaling promotes colorectal cancer stemness and malignancy in an acidic microenvironment. Signal Transduct. Target. Ther. 5(1), 183 (2020).
  Medline CASGoogle Scholar
• 135. Hu P, Li S, Tian N et al. Acidosis enhances the self-renewal and mitochondrial respiration of stem cell-like glioma cells through CYP24A1-mediated reduction of vitamin D. Cell Death Dis. 10(1), 25 (2019).
  Medline CASGoogle Scholar
• 136. Detich N, Hamm S, Just G, Knox JD, Szyf M. The methyl donor S-adenosylmethionine inhibits active demethylation of DNA: a candidate novel mechanism for the pharmacological effects of S-Adenosylmethionine. J. Biol. Chem. 278(23), 20812–20820 (2003).
  Medline CASGoogle Scholar
• 137. Mukhopadhyay S. Familial manganese-induced neurotoxicity due to mutations in SLC30A10 or SLC39A14. Neurotoxicology 64, 278–283 (2018).
  Medline CASGoogle Scholar
• 138. Tuschl K, Mills PB, Parsons H et al. Hepatic cirrhosis, dystonia, polycythaemia and hypermanganesaemia – a new metabolic disorder. J. Inherit. Metab. Dis. 31(2), 151–163 (2008).
  Medline CASGoogle Scholar
• 139. Claro Da Silva T, Hiller C, Gai Z, Kullak-Ublick GA. Vitamin D3 transactivates the zinc and manganese transporter SLC30A10 via the Vitamin D receptor. J. Steroid Biochem. Mol. Biol. 163, 77–87 (2016).
  MedlineGoogle Scholar
• 140. Hutchens S, Liu C, Jursa T et al. Deficiency in the manganese efflux transporter SLC30A10 induces severe hypothyroidism in mice. J. Biol. Chem. 292(23), 9760–9773 (2017).
  Medline CASGoogle Scholar
• 141. Li S, De La Cruz J, Christakos S et al. Nutrigenomics of 1, 25 (OH) 2D3 action in the intestine: evidence for a role of 1, 25 (OH) 2D3 in manganese transport. J. Bone Miner. Res. 34, 212 (2019).
  Google Scholar
• 142. Li S, De La Cruz J, Hutchens S et al. Analysis of 1,25-dihydroxyvitamin D(3) genomic action reveals calcium-regulating and calcium-independent effects in mouse intestine and human enteroids. Mol. Cell. Biol. 41(1), e00372–20 (2020).
  Medline CASGoogle Scholar
• 143. Christakos S, Li S, De La Cruz J et al. Vitamin D and the intestine: review and update. J. Steroid Biochem. Mol. Biol. 196, 105501 (2020).
  Medline CASGoogle Scholar
• 144. Ahmad TR, Higuchi S, Bertaggia E et al. Bile acid composition regulates the manganese transporter Slc30a10 in intestine. J. Biol. Chem. 295(35), 12545–12558 (2020).
  Medline CASGoogle Scholar
• 145. Kawamata Y, Fujii R, Hosoya M et al. A G protein-coupled receptor responsive to bile acids. J. Biol. Chem. 278(11), 9435–9440 (2003).
  Medline CASGoogle Scholar
• 146. Maruyama T, Miyamoto Y, Nakamura T et al. Identification of membrane-type receptor for bile acids (M-BAR). Biochem. Biophys. Res. Commun. 298(5), 714–719 (2002).
  Medline CASGoogle Scholar
• 147. Kerachian MA, Javadmanesh A, Azghandi M et al. Crosstalk between DNA methylation and gene expression in colorectal cancer, a potential plasma biomarker for tracing this tumor. Sci. Rep. 10(1), 2813 (2020).
  Medline CASGoogle Scholar
• 148. Yagi K, Akagi K, Hayashi H et al. Three DNA methylation epigenotypes in human colorectal cancer. Clin. Cancer Res. 16(1), 21–33 (2010).
  Medline CASGoogle Scholar
• 149. Shangkuan WC, Lin HC, Chang YT et al. Risk analysis of colorectal cancer incidence by gene expression analysis. PeerJ 5, e3003 (2017).
  MedlineGoogle Scholar
• 150. Shukeir N, Stefanska B, Parashar S et al. Pharmacological methyl group donors block skeletal metastasis in vitro and in vivo. Br. J. Pharmacol. 172(11), 2769–2781 (2015).
  Medline CASGoogle Scholar
• 151. Parashar S, Cheishvili D, Arakelian A et al. S-adenosylmethionine blocks osteosarcoma cells proliferation and invasion in vitro and tumor metastasis in vivo: therapeutic and diagnostic clinical applications. Cancer Med. 4(5), 732–744 (2015).
  Medline CASGoogle Scholar
• 152. Mehdi A, Attias M, Mahmood N et al. Enhanced anticancer effect of a combination of S-adenosylmethionine (SAM) and immune checkpoint inhibitor (ICPi) in a syngeneic mouse model of advanced melanoma. Front. Oncol. 10, 1361 (2020).
  MedlineGoogle Scholar
• 153. Mahmood N, Cheishvili D, Arakelian A et al. Methyl donor S-adenosylmethionine (SAM) supplementation attenuates breast cancer growth, invasion, and metastasis in vivo; therapeutic and chemopreventive applications. Oncotarget 9(4), 5169–5183 (2018).
  MedlineGoogle Scholar
• 154. Mahmood N, Arakelian A, Cheishvili D, Szyf M, Rabbani SA. S-adenosylmethionine in combination with decitabine shows enhanced anti-cancer effects in repressing breast cancer growth and metastasis. J. Cell. Mol. Med. 24(18), 10322–10337 (2020).
  Medline CASGoogle Scholar
• 155. Larriba MJ, Muñoz A. SNAIL vs vitamin D receptor expression in colon cancer: therapeutics implications. Br. J. Cancer 92(6), 985–989 (2005).
  Medline CASGoogle Scholar
• 156. Bhatia V, Falzon M. Restoration of the anti-proliferative and anti-migratory effects of 1,25-dihydroxyvitamin D by silibinin in vitamin D-resistant colon cancer cells. Cancer Lett. 362(2), 199–207 (2015).
  Medline CASGoogle Scholar