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Current Opinion in Molecular Pathology of Ameloblastoma: A Literature Review

  • Dong‑Joon, Lee (Division in Anatomy and Developmental Biology, Department of Oral Biology, Taste Research Center, Oral Science Research Center, BK21 FOUR Project, Yonsei University College of Dentistry) ;
  • Shujin, Li (Division in Anatomy and Developmental Biology, Department of Oral Biology, Taste Research Center, Oral Science Research Center, BK21 FOUR Project, Yonsei University College of Dentistry) ;
  • Han‑Sung, Jung (Division in Anatomy and Developmental Biology, Department of Oral Biology, Taste Research Center, Oral Science Research Center, BK21 FOUR Project, Yonsei University College of Dentistry)
  • 투고 : 2022.12.09
  • 심사 : 2022.12.14
  • 발행 : 2022.12.30

초록

Ameloblastoma is the most representative epithelial odontogenic tumor in the craniofacial region. Through several studies on Ameloblastoma that have been conducted so far, we have been able to get closer to the reality of Ameloblastoma. However, groundbreaking insight into the pathophysiology of Ameloblastoma has not yet been provided. This review assessed three aspects of five recently published papers on Ameloblastoma: cancer stem cells, calcium signaling, and tumor microenvironment, and compared them with previous studies on tumor physiology, including cancer. In addition, the characteristics of Ameloblastoma revealed by the experimental methods presented in the currently published five papers provide the possibility of Ameloblastoma as a study model in general tumor or cancer studies. Furthermore, the mechanisms of action of the chemicals identified in the studies support their potential as candidates for the second-line treatment of Ameloblastoma.

키워드

과제정보

The assistance in English correction of Anish Ashok Adpaikar (Yonsei University College of Dentistry) is gratefully acknowledged. This research was supported by the Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education (NRF-2022R1I1A1A01071838). This research was also supported by the NRF grant funded by the Korea Government (MSIP) (NRF-2022R1A2B5B03001627, NRF-2016R1A5A2008630).

참고문헌

  1. Gardner DG. Some current concepts on the pathology of ameloblastomas. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 1996; 82: 660-9. https://doi.org/10.1016/S1079-2104(96)80441-0
  2. Maia Campos G. Ameloblastoma, a behavioral and histologic paradox (a philosophical approach). Braz Dent J. 1990; 1: 5-15.
  3. Morgan PR. Odontogenic tumors: a review. Periodontol 2000. 2011; 57: 160-76. https://doi.org/10.1111/j.1600-0757.2011.00393.x
  4. Masthan KM, Anitha N, Krupaa J, Manikkam S. Ameloblastoma. J Pharm Bioallied Sci. 2015; 7(Suppl 1): S167-70.
  5. Thompson L. World Health Organization classification of tumours: pathology and genetics of head and neck tumours. Ear Nose Throat J. 2006; 85: 74. https://doi.org/10.1177/014556130608500201
  6. Diniz MG, Gomes CC, de Sousa SF, Xavier GM, Gomez RS. Oncogenic signalling pathways in benign odontogenic cysts and tumours. Oral Oncol. 2017; 72: 165-73. https://doi.org/10.1016/j.oraloncology.2017.07.021
  7. Gorlin RJ, Chaudhry AP, Pindborg JJ. Odontogenic tumors. Classification, histopathology, and clinical behavior in man and domesticated animals. Cancer. 1961; 14: 73-101. https://doi.org/10.1002/1097-0142(196101/02)14:1<73::AID-CNCR2820140111>3.0.CO;2-T
  8. Brown NA, Rolland D, McHugh JB, Weigelin HC, Zhao L, Lim MS, Elenitoba-Johnson KS, Betz BL. Activating FGFR2-RAS-BRAF mutations in ameloblastoma. Clin Cancer Res. 2014; 20: 5517-26. https://doi.org/10.1158/1078-0432.CCR-14-1069
  9. Farias LC, Gomes CC, Brito JA, Galvao CF, Diniz MG, de Castro WH, Bernardes Vde F, De Marco LA, Gomez RS. Loss of heterozygosity of the PTCH gene in ameloblastoma. Hum Pathol. 2012; 43: 1229-33. https://doi.org/10.1016/j.humpath.2011.08.026
  10. Gomes CC, de Sousa SF, de Menezes GH, Duarte AP, Pereira Tdos S, Moreira RG, de Castro WH, Villacis RA, Rogatto SR, Diniz MG, Gomez RS. Recurrent KRAS G12V pathogenic mutation in adenomatoid odontogenic tumours. Oral Oncol. 2016; 56: e3-5. https://doi.org/10.1016/j.oraloncology.2016.03.001
  11. Gurgel CA, Buim ME, Carvalho KC, Sales CB, Reis MG, de Souza RO, de Faro Valverde L, de Azevedo RA, Dos Santos JN, Soares FA, Ramos EA. Transcriptional profiles of SHH pathway genes in keratocystic odontogenic tumor and ameloblastoma. J Oral Pathol Med. 2014; 43: 619-26. https://doi.org/10.1111/jop.12180
  12. Harada H, Mitsuyasu T, Nakamura N, Higuchi Y, Toyoshima K, Taniguchi A, Yasumoto S. Establishment of ameloblastoma cell line, AM-1. J Oral Pathol Med. 1998; 27: 207-12.
  13. Sandra F, Hendarmin L, Kukita T, Nakao Y, Nakamura N, Nakamura S. Ameloblastoma induces osteoclastogenesis: a possible role of ameloblastoma in expanding in the bone. Oral Oncol. 2005; 41: 637-44. https://doi.org/10.1016/j.oraloncology.2005.02.008
  14. Yoshimoto S, Morita H, Matsubara R, Mitsuyasu T, Imai Y, Kajioka S, Yoneda M, Ito Y, Hirofuji T, Nakamura S, Hirata M. Surface vacuolar ATPase in ameloblastoma contributes to tumor invasion of the jaw bone. Int J Oncol. 2016; 48: 1258-70. https://doi.org/10.3892/ijo.2016.3350
  15. Chang TH, Shanti RM, Liang Y, Zeng J, Shi S, Alawi F, Carrasco L, Zhang Q, Le AD. LGR5+ epithelial tumor stem-like cells generate a 3D-organoid model for ameloblastoma. Cell Death Dis. 2020; 11: 338. https://doi.org/10.1038/s41419-020-2560-7
  16. Lawson DA, Kessenbrock K, Davis RT, Pervolarakis N, Werb Z. Tumour heterogeneity and metastasis at single-cell resolution. Nat Cell Biol. 2018; 20: 1349-60. https://doi.org/10.1038/s41556-018-0236-7
  17. Ponomarev A, Gilazieva Z, Solovyeva V, Allegrucci C, Rizvanov A. Intrinsic and extrinsic factors impacting cancer stemness and tumor progression. Cancers (Basel). 2022; 14: 970. https://doi.org/10.3390/cancers14040970
  18. Marusyk A, Almendro V, Polyak K. Intra-tumour heterogeneity: a looking glass for cancer? Nat Rev Cancer. 2012; 12: 323-34. https://doi.org/10.1038/nrc3261
  19. McGranahan N, Furness AJ, Rosenthal R, Ramskov S, Lyngaa R, Saini SK, Jamal-Hanjani M, Wilson GA, Birkbak NJ, Hiley CT, Watkins TB, Shafi S, Murugaesu N, Mitter R, Akarca AU, Linares J, Marafioti T, Henry JY, Van Allen EM, Miao D, Schilling B, Schadendorf D, Garraway LA, Makarov V, Rizvi NA, Snyder A, Hellmann MD, Merghoub T, Wolchok JD, Shukla SA, Wu CJ, Peggs KS, Chan TA, Hadrup SR, Quezada SA, Swanton C. Clonal neoantigens elicit T cell immunoreactivity and sensitivity to immune checkpoint blockade. Science. 2016; 351: 1463-9. https://doi.org/10.1126/science.aaf1490
  20. van Niekerk G, Davids LM, Hattingh SM, Engelbrecht AM. Cancer stem cells: a product of clonal evolution? Int J Cancer. 2017; 140: 993-9. https://doi.org/10.1002/ijc.30448
  21. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011; 144: 646-74. https://doi.org/10.1016/j.cell.2011.02.013
  22. Morel AP, Lievre M, Thomas C, Hinkal G, Ansieau S, Puisieux A. Generation of breast cancer stem cells through epithelial-mesenchymal transition. PLoS One. 2008; 3: e2888. https://doi.org/10.1371/journal.pone.0002888
  23. Singh A, Settleman J. EMT, cancer stem cells and drug resistance: an emerging axis of evil in the war on cancer. Oncogene. 2010; 29: 4741-51. https://doi.org/10.1038/onc.2010.215
  24. Boumahdi S, Driessens G, Lapouge G, Rorive S, Nassar D, Le Mercier M, Delatte B, Caauwe A, Lenglez S, Nkusi E, Brohee S, Salmon I, Dubois C, del Marmol V, Fuks F, Beck B, Blanpain C. SOX2 controls tumour initiation and cancer stem-cell functions in squamous-cell carcinoma. Nature. 2014; 511: 246-50. https://doi.org/10.1038/nature13305
  25. Kim HY, Li S, Lee DJ, Park JH, Muramatsu T, Harada H, Jung YS, Jung HS. Activation of Wnt signalling reduces the population of cancer stem cells in ameloblastoma. Cell Prolif. 2021; 54: e13073. https://doi.org/10.1111/cpr.13073
  26. Hendarmin L, Sandra F, Nakao Y, Ohishi M, Nakamura N. TNFalpha played a role in induction of Akt and MAPK signals in ameloblastoma. Oral Oncol. 2005; 41: 375-82. https://doi.org/10.1016/j.oraloncology.2004.09.014
  27. Kanda S, Mitsuyasu T, Nakao Y, Kawano S, Goto Y, Matsubara R, Nakamura S. Anti-apoptotic role of the sonic hedgehog signaling pathway in the proliferation of ameloblastoma. Int J Oncol. 2013; 43: 695-702. https://doi.org/10.3892/ijo.2013.2010
  28. Sandra F, Hendarmin L, Nakao Y, Nakamura N, Nakamura S. Inhibition of Akt and MAPK pathways elevated potential of TNFalpha in inducing apoptosis in ameloblastoma. Oral Oncol. 2006; 42: 39-45.
  29. Sathi GA, Inoue M, Harada H, Rodriguez AP, Tamamura R, Tsujigiwa H, Borkosky SS, Gunduz M, Nagatsuka H. Secreted frizzled related protein (sFRP)-2 inhibits bone formation and promotes cell proliferation in ameloblastoma. Oral Oncol. 2009; 45: 856-60. https://doi.org/10.1016/j.oraloncology.2009.02.001
  30. Sathi GA, Tsujigiwa H, Ito S, Siar CH, Katase N, Tamamura R, Harada H, Nagatsuka H. Osteogenic genes related to the canonic WNT pathway are down-regulated in ameloblastoma. Oral Surg Oral Med Oral Pathol Oral Radiol. 2012; 114: 771-7. https://doi.org/10.1016/j.oooo.2012.08.453
  31. Cheung KJ, Ewald AJ. A collective route to metastasis: seeding by tumor cell clusters. Science. 2016; 352: 167-9. https://doi.org/10.1126/science.aaf6546
  32. Friedl P, Locker J, Sahai E, Segall JE. Classifying collective cancer cell invasion. Nat Cell Biol. 2012; 14: 777-83. https://doi.org/10.1038/ncb2548
  33. Chrisafis G, Wang T, Moissoglu K, Gasparski AN, Ng Y, Weigert R, Lockett SJ, Mili S. Collective cancer cell invasion requires RNA accumulation at the invasive front. Proc Natl Acad Sci U S A. 2020; 117: 27423-34. https://doi.org/10.1073/pnas.2010872117
  34. Grasset EM, Bertero T, Bozec A, Friard J, Bourget I, Pisano S, Lecacheur M, Maiel M, Bailleux C, Emelyanov A, Ilie M, Hofman P, Meneguzzi G, Duranton C, Bulavin DV, Gaggioli C. Matrix stiffening and EGFR cooperate to promote the collective invasion of cancer cells. Cancer Res. 2018; 78: 5229-42. https://doi.org/10.1158/0008-5472.CAN-18-0601
  35. Iamshanova O, Fiorio Pla A, Prevarskaya N. Molecular mechanisms of tumour invasion: regulation by calcium signals. J Physiol. 2017; 595: 3063-75. https://doi.org/10.1113/JP272844
  36. Berridge MJ, Lipp P, Bootman MD. The versatility and universality of calcium signalling. Nat Rev Mol Cell Biol. 2000; 1: 11-21. https://doi.org/10.1038/35036035
  37. Xu M, Seas A, Kiyani M, Ji KSY, Bell HN. A temporal examination of calcium signaling in cancer- from tumorigenesis, to immune evasion, and metastasis. Cell Biosci. 2018; 8: 25. https://doi.org/10.1186/s13578-018-0223-5
  38. Sharma S, Wu SY, Jimenez H, Xing F, Zhu D, Liu Y, Wu K, Tyagi A, Zhao D, Lo HW, Metheny-Barlow L, Sun P, Bourland JD, Chan MD, Thomas A, Barbault A, D'Agostino RB, Whitlow CT, Kirchner V, Blackman C, Pasche B, Watabe K. Ca2+ and CACNA1H mediate targeted suppression of breast cancer brain metastasis by AM RF EMF. EBioMedicine. 2019; 44: 194-208. https://doi.org/10.1016/j.ebiom.2019.05.038
  39. Jacquemet G, Baghirov H, Georgiadou M, Sihto H, Peuhu E, Cettour-Janet P, He T, Perala M, Kronqvist P, Joensuu H, Ivaska J. L-type calcium channels regulate filopodia stability and cancer cell invasion downstream of integrin signalling. Nat Commun. 2016; 7: 13297. https://doi.org/10.1038/ncomms13297
  40. Li S, Kim HY, Lee DJ, Park SH, Otsu K, Harada H, Jung YS, Jung HS. Inhibition of L-type voltage-gated calcium channel-mediated Ca2+ influx suppresses the collective migration and invasion of ameloblastoma. Cell Prolif. 2022; 55: e13305. https://doi.org/10.1111/cpr.13305
  41. Li S, Lee DJ, Kim HY, Kim JY, Jung YS, Jung HS. Unraveled roles of Cav1.2 in proliferation and stemness of ameloblastoma. Cell Biosci. 2022; 12: 145. https://doi.org/10.1186/s13578-022-00873-9
  42. Vinci M, Gowan S, Boxall F, Patterson L, Zimmermann M, Court W, Lomas C, Mendiola M, Hardisson D, Eccles SA. Advances in establishment and analysis of three-dimensional tumor spheroid-based functional assays for target validation and drug evaluation. BMC Biol. 2012; 10: 29. https://doi.org/10.1186/1741-7007-10-29
  43. Popp T, Steinritz D, Breit A, Deppe J, Egea V, Schmidt A, Gudermann T, Weber C, Ries C. Wnt5a/β-catenin signaling drives calcium-induced differentiation of human primary keratinocytes. J Invest Dermatol. 2014; 134: 2183-91. https://doi.org/10.1038/jid.2014.149
  44. Thrasivoulou C, Millar M, Ahmed A. Activation of intracellular calcium by multiple Wnt ligands and translocation of β-catenin into the nucleus: a convergent model of Wnt/Ca2+ and Wnt/β-catenin pathways. J Biol Chem. 2013; 288: 35651-9. https://doi.org/10.1074/jbc.M112.437913
  45. Park YJ, Yoo SA, Kim M, Kim WU. The role of calcium-calcineurin-NFAT signaling pathway in health and autoimmune diseases. Front Immunol. 2020; 11: 195. https://doi.org/10.3389/fimmu.2020.00195
  46. Zaslavsky A, Chou ST, Schadler K, Lieberman A, Pimkin M, Kim YJ, Baek KH, Aird WC, Weiss MJ, Ryeom S. The calcineurin-NFAT pathway negatively regulates megakaryopoiesis. Blood. 2013; 121: 3205-15. https://doi.org/10.1182/blood-2012-04-421172
  47. Li L, Duan Z, Yu J, Dang HX. NFATc1 regulates cell proliferation, migration, and invasion of ovarian cancer SKOV3 cells in vitro and in vivo. Oncol Rep. 2016; 36: 918-28. https://doi.org/10.3892/or.2016.4904
  48. Xu W, Gu J, Ren Q, Shi Y, Xia Q, Wang J, Wang S, Wang Y, Wang J. NFATC1 promotes cell growth and tumorigenesis in ovarian cancer up-regulating c-Myc through ERK1/2/p38 MAPK signal pathway. Tumour Biol. 2016; 37: 4493-500. https://doi.org/10.1007/s13277-015-4245-x
  49. Peuker K, Muff S, Wang J, Kunzel S, Bosse E, Zeissig Y, Luzzi G, Basic M, Strigli A, Ulbricht A, Kaser A, Arlt A, Chavakis T, van den Brink GR, Schafmayer C, Egberts JH, Becker T, Bianchi ME, Bleich A, Rocken C, Hampe J, Schreiber S, Baines JF, Blumberg RS, Zeissig S. Epithelial calcineurin controls microbiota-dependent intestinal tumor development. Nat Med. 2016; 22: 506-15. https://doi.org/10.1038/nm.4072
  50. Poltavets V, Kochetkova M, Pitson SM, Samuel MS. The role of the extracellular matrix and its molecular and cellular regulators in cancer cell plasticity. Front Oncol. 2018; 8: 431. https://doi.org/10.3389/fonc.2018.00431
  51. Nallanthighal S, Heiserman JP, Cheon DJ. The role of the extracellular matrix in cancer stemness. Front Cell Dev Biol. 2019; 7: 86.
  52. Gilkes DM, Semenza GL, Wirtz D. Hypoxia and the extracellular matrix: drivers of tumour metastasis. Nat Rev Cancer. 2014; 14: 430-9. https://doi.org/10.1038/nrc3726
  53. Xu S, Xu H, Wang W, Li S, Li H, Li T, Zhang W, Yu X, Liu L. The role of collagen in cancer: from bench to bedside. J Transl Med. 2019; 17: 309. https://doi.org/10.1186/s12967-019-2058-1
  54. Jia H, Janjanam J, Wu SC, Wang R, Pano G, Celestine M, Martinot O, Breeze-Jones H, Clayton G, Garcin C, Shirinifard A, Zaske AM, Finkelstein D, Labelle M. The tumor cell-secreted matricellular protein WISP1 drives pro-metastatic collagen linearization. EMBO J. 2019; 38: e101302. https://doi.org/10.15252/embj.2018101302
  55. Pure E, Blomberg R. Pro-tumorigenic roles of fibroblast activation protein in cancer: back to the basics. Oncogene. 2018; 37: 4343-57. https://doi.org/10.1038/s41388-018-0275-3
  56. Venning FA, Wullkopf L, Erler JT. Targeting ECM disrupts cancer progression. Front Oncol. 2015; 5: 224. https://doi.org/10.3389/fonc.2015.00224
  57. da Rosa MR, Falcao AS, Fuzii HT, da Silva Kataoka MS, Ribeiro AL, Boccardo E, de Siqueira AS, Jaeger RG, de Jesus Viana Pinheiro J, de Melo Alves Junior S. EGFR signaling downstream of EGF regulates migration, invasion, and MMP secretion of immortalized cells derived from human ameloblastoma. Tumour Biol. 2014; 35: 11107-20. https://doi.org/10.1007/s13277-014-2401-3
  58. Li S, Lee DJ, Kim HY, Harada H, Jung YS, Jung HS. Transcriptomic comparison analysis between ameloblastoma and AM-1 Cell line. Int J Stem Cells. 2022; 15: 415-21. https://doi.org/10.15283/ijsc22132
  59. Li S, Lee DJ, Kim HY, Kim JY, Jung YS, Jung HS. Ameloblastoma modifies tumor microenvironment for enhancing invasiveness by altering collagen alignment. Histochem Cell Biol. 2022; 158: 595-602. https://doi.org/10.1007/s00418-022-02136-7
  60. Gong X, Kulwatno J, Mills KL. Rapid fabrication of collagen bundles mimicking tumor-associated collagen architectures. Acta Biomater. 2020; 108: 128-41. https://doi.org/10.1016/j.actbio.2020.03.019
  61. Effiom OA, Ogundana OM, Akinshipo AO, Akintoye SO. Ameloblastoma: current etiopathological concepts and management. Oral Dis. 2018; 24: 307-16. https://doi.org/10.1111/odi.12646
  62. Sweeney RT, McClary AC, Myers BR, Biscocho J, Neahring L, Kwei KA, Qu K, Gong X, Ng T, Jones CD, Varma S, Odegaard JI, Sugiyama T, Koyota S, Rubin BP, Troxell ML, Pelham RJ, Zehnder JL, Beachy PA, Pollack JR, West RB. Identification of recurrent SMO and BRAF mutations in ameloblastomas. Nat Genet. 2014; 46: 722-5. Erratum in: Nat Genet. 2015; 47: 97.
  63. Carnero A, Garcia-Mayea Y, Mir C, Lorente J, Rubio IT, LLeonart ME. The cancer stem-cell signaling network and resistance to therapy. Cancer Treat Rev. 2016; 49: 25-36. https://doi.org/10.1016/j.ctrv.2016.07.001
  64. Heikinheimo K, Kurppa KJ, Elenius K. Novel targets for the treatment of ameloblastoma. J Dent Res. 2015; 94: 237-40.