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Erschienen in: Clinical Oral Investigations 1/2018

25.02.2017 | Original Article

Role of HIF-1α and CASPASE-3 in cystogenesis of odontogenic cysts and tumors

verfasst von: Natacha M. M. da Costa, Adriane S. de Siqueira, André L. R. Ribeiro, Maria S. da Silva Kataoka, Ruy G. Jaeger, Sérgio M. de Alves-Júnior, Andrew M. Smith, João de Jesus Viana Pinheiro

Erschienen in: Clinical Oral Investigations | Ausgabe 1/2018

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Abstract

Objectives

Odontogenic cysts and tumors are the most relevant lesions that affect the gnathic bones. These lesions have in common the formation of cystic areas and this common feature may suggest involvement of similar mechanisms. The hypoxia inducible factor 1 alpha (HIF-1α), a responsive protein to hypoxia and caspase-3, an irreversible apoptosis marker, may contribute to cyst formation. Thus, this study aimed to investigate the immunoexpression of these proteins in odontogenic cysts and tumors.

Material and methods

Twenty cases of ameloblastoma, keratocystic odontogenic tumor (KOT) (n = 20), radicular cyst (RC) (n = 18), dentigerous cyst (DC) (n = 11), calcifying cystic odontogenic tumor (n = 8), and dental follicle (DF) (n = 10) were used to investigate HIF-1α and caspase-3 expression in sequential serial cuts by immunohistochemistry.

Results

HIF-1α was overexpressed in RC, DC, and ameloblastoma when compared with DF. The basal and sometimes the lower suprabasal layer showed no or very low expression in DC, KOT, and ameloblastoma, the last also showing strong expression in solid epithelial areas and initial cystic formation regions. Caspase-3 was found to be overexpressed in all lesions, with the highest expression in odontogenic cysts compared to tumors. HIF-1α and caspase-3 were localized in similar areas of the same lesions, especially in the epithelium surrounding cystic formations.

Conclusions

This study showed distinct immunoexpression of HIF-1α and caspase-3 in odontogenic cyst and tumors, with higher expression observed in odontogenic cysts.

Clinical relevance

These findings suggest a possible correlation between hypoxia, apoptosis, and cystogenesis, leading to understand the mechanisms responsible to cystic formation in odontogenic lesions.
Literatur
1.
Zurück zum Zitat Sciubba JJ, Fantasia JE, Kahn LB (2000) Atlas of tumor pathology. Tumors and cyst of jaw. AFIP, Washington DC Sciubba JJ, Fantasia JE, Kahn LB (2000) Atlas of tumor pathology. Tumors and cyst of jaw. AFIP, Washington DC
2.
Zurück zum Zitat Barnes L, Eveson JW, Reichart P, Sidransky D (2005) World Health Organization classification of tumors. Pathology and genetics of head and neck tumours, 9th edn. IARC Press, Lyon, pp 296–300 Barnes L, Eveson JW, Reichart P, Sidransky D (2005) World Health Organization classification of tumors. Pathology and genetics of head and neck tumours, 9th edn. IARC Press, Lyon, pp 296–300
3.
Zurück zum Zitat Rapidis AD, Andressakis DD, Stavrianos SD, Faratzis G, Arnogiannaki-Liappi N, Lagogiannis GA, Valsamis SV, Apostolikas N (2004) Ameloblastomas of the jaws: clinico-pathological review of 11 patients. Eur J Surg Oncol 30:998–1002CrossRefPubMed Rapidis AD, Andressakis DD, Stavrianos SD, Faratzis G, Arnogiannaki-Liappi N, Lagogiannis GA, Valsamis SV, Apostolikas N (2004) Ameloblastomas of the jaws: clinico-pathological review of 11 patients. Eur J Surg Oncol 30:998–1002CrossRefPubMed
4.
Zurück zum Zitat Reichart PA, Philipsen HP, Sonner S (1995) Ameloblastoma: biological profile of 3677 cases. Eur J Cancer B Oral Oncol 31B:86–99CrossRefPubMed Reichart PA, Philipsen HP, Sonner S (1995) Ameloblastoma: biological profile of 3677 cases. Eur J Cancer B Oral Oncol 31B:86–99CrossRefPubMed
5.
Zurück zum Zitat Chirapathomsakul D, Sastravaha P, Jansisyanont P (2006) A review of odontogenic keratocysts and the behavior of recurrences. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 101:5–9CrossRefPubMed Chirapathomsakul D, Sastravaha P, Jansisyanont P (2006) A review of odontogenic keratocysts and the behavior of recurrences. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 101:5–9CrossRefPubMed
6.
Zurück zum Zitat Shear M, Speight P (2007) Cysts of the oral and maxillofacil regions. Wright, OxfordCrossRef Shear M, Speight P (2007) Cysts of the oral and maxillofacil regions. Wright, OxfordCrossRef
7.
Zurück zum Zitat Ward JP, Magar V, Franks SJ, Landini G (2004) A mathematical model of the dynamics of odontogenic cyst growth. Anal Quant Cytol Histol 26:39–46PubMed Ward JP, Magar V, Franks SJ, Landini G (2004) A mathematical model of the dynamics of odontogenic cyst growth. Anal Quant Cytol Histol 26:39–46PubMed
8.
Zurück zum Zitat Piattelli A, Fioroni M, Santinelli A, Rubini C (1998) Expression of proliferating cell nuclear antigen in ameloblastomas and odontogenic cysts. Oral Oncol 34:408–412CrossRefPubMed Piattelli A, Fioroni M, Santinelli A, Rubini C (1998) Expression of proliferating cell nuclear antigen in ameloblastomas and odontogenic cysts. Oral Oncol 34:408–412CrossRefPubMed
9.
Zurück zum Zitat Lin LM, Huang GT, Rosenberg PA (2007) Proliferation of epithelial cell rests, formation of apical cysts, and regression of apical cysts after periapical wound healing. J Endod 33:908–916CrossRefPubMed Lin LM, Huang GT, Rosenberg PA (2007) Proliferation of epithelial cell rests, formation of apical cysts, and regression of apical cysts after periapical wound healing. J Endod 33:908–916CrossRefPubMed
10.
Zurück zum Zitat Dag O, Ford TRP (1998) Essential Endodontology: prevention and Tratament of apical periodontitis, 1st edn. Blackwell Science, Oxford, pp 68–105 Dag O, Ford TRP (1998) Essential Endodontology: prevention and Tratament of apical periodontitis, 1st edn. Blackwell Science, Oxford, pp 68–105
11.
Zurück zum Zitat Ten Cate AR (1972) The epithelial cell rests of Malassez and the genesis of the dental cyst. Oral Surg Oral Med Oral Pathol 34:956–964CrossRefPubMed Ten Cate AR (1972) The epithelial cell rests of Malassez and the genesis of the dental cyst. Oral Surg Oral Med Oral Pathol 34:956–964CrossRefPubMed
13.
Zurück zum Zitat Thosaporn W, Iamaroon A, Pongsiriwet S, Ng KH (2004) A comparative study of epithelial cell proliferation between the odontogenic keratocyst, orthokeratinized odontogenic cyst, dentigerous cyst, and ameloblastoma. Oral Dis 10:22–26CrossRefPubMed Thosaporn W, Iamaroon A, Pongsiriwet S, Ng KH (2004) A comparative study of epithelial cell proliferation between the odontogenic keratocyst, orthokeratinized odontogenic cyst, dentigerous cyst, and ameloblastoma. Oral Dis 10:22–26CrossRefPubMed
14.
Zurück zum Zitat Seifi S, Shafigh E, Allaie A (2011) Quantitative and qualitative analysis of argyrophilic nuclear organizer regions in follicular cyst, keratocystic odontogenic tumor and ameloblastoma. J Cancer Res Ther 7:280–285CrossRefPubMed Seifi S, Shafigh E, Allaie A (2011) Quantitative and qualitative analysis of argyrophilic nuclear organizer regions in follicular cyst, keratocystic odontogenic tumor and ameloblastoma. J Cancer Res Ther 7:280–285CrossRefPubMed
15.
Zurück zum Zitat Martins CA, Rivero ER, Dufloth RM, Figueiredo CP, Vieira DS (2011) Immunohistochemical detection of factors related to cellular proliferation and apoptosis in radicular and dentigerous cysts. J Endod 37:36–39CrossRefPubMed Martins CA, Rivero ER, Dufloth RM, Figueiredo CP, Vieira DS (2011) Immunohistochemical detection of factors related to cellular proliferation and apoptosis in radicular and dentigerous cysts. J Endod 37:36–39CrossRefPubMed
16.
Zurück zum Zitat Kefalides NA, Borel JP (2005) Basement membranes: cell and molecular biology. Academic Press, California Kefalides NA, Borel JP (2005) Basement membranes: cell and molecular biology. Academic Press, California
17.
Zurück zum Zitat Hammond EM, Asselin MC, Forster D, O'Connor JP, Senra JM, Williams KJ (2014) The meaning, measurement and modification of hypoxia in the laboratory and the clinic. Clin Oncol 26:277–288CrossRef Hammond EM, Asselin MC, Forster D, O'Connor JP, Senra JM, Williams KJ (2014) The meaning, measurement and modification of hypoxia in the laboratory and the clinic. Clin Oncol 26:277–288CrossRef
18.
Zurück zum Zitat Kieda C, Greferath R, Crola da Silva C, Fylaktakidou KC, Lehn JM, Nicolau C (2006) Suppression of hypoxia-induced HIF-1alpha and of angiogenesis in endothelial cells by myo-inositol trispyrophosphate-treated erythrocytes. Proc Natl Acad Sci U S A 103:15576–15581CrossRefPubMedPubMedCentral Kieda C, Greferath R, Crola da Silva C, Fylaktakidou KC, Lehn JM, Nicolau C (2006) Suppression of hypoxia-induced HIF-1alpha and of angiogenesis in endothelial cells by myo-inositol trispyrophosphate-treated erythrocytes. Proc Natl Acad Sci U S A 103:15576–15581CrossRefPubMedPubMedCentral
19.
Zurück zum Zitat Lee JW, Bae SH, Jeong JW, Kim SH, Kim KW (2004) Hypoxia-inducible factor (HIF-1) alpha: its protein stability and biological functions. Exp Mol Med 36:1–12CrossRefPubMed Lee JW, Bae SH, Jeong JW, Kim SH, Kim KW (2004) Hypoxia-inducible factor (HIF-1) alpha: its protein stability and biological functions. Exp Mol Med 36:1–12CrossRefPubMed
20.
Zurück zum Zitat Wang GL, Semenza GL (1995) Purification and characterization of hypoxia-inducible factor 1. J Biol Chem 270:1230–1237CrossRefPubMed Wang GL, Semenza GL (1995) Purification and characterization of hypoxia-inducible factor 1. J Biol Chem 270:1230–1237CrossRefPubMed
21.
Zurück zum Zitat Maxwell P (2003) Hif-1: an oxygen response system with special relevance to the kidney. J Am Soc Nephrol 14:2712–2722CrossRefPubMed Maxwell P (2003) Hif-1: an oxygen response system with special relevance to the kidney. J Am Soc Nephrol 14:2712–2722CrossRefPubMed
22.
Zurück zum Zitat Edelstein CL (2005) What is the role of tubular epithelial cell apoptosis in polycystic kidney disease (pkd)? Cell Cycle 4:1550–1554CrossRefPubMed Edelstein CL (2005) What is the role of tubular epithelial cell apoptosis in polycystic kidney disease (pkd)? Cell Cycle 4:1550–1554CrossRefPubMed
23.
Zurück zum Zitat Amaral FR, Mateus GC, Bonisson LA, de Andrade BA, Mesquita RA, Horta MC, Marigo Hde A (2012) Cell proliferation and apoptosis in ameloblastomas and keratocystic odontogenic tumors. Braz Dent J 23:91–96CrossRefPubMed Amaral FR, Mateus GC, Bonisson LA, de Andrade BA, Mesquita RA, Horta MC, Marigo Hde A (2012) Cell proliferation and apoptosis in ameloblastomas and keratocystic odontogenic tumors. Braz Dent J 23:91–96CrossRefPubMed
24.
Zurück zum Zitat Da Costa NM, Fialho AD, Proietti CC, da Silva Kataoka MS, Jaeger RG, de Alves-Junior SM, de Jesus Viana Pinheiro J (2016) Role of hypoxia-related proteins in invasion of ameloblastoma cells: crosstalk between NOTCH1, hypoxia-inducible factor 1alpha, a disintegrin and metalloproteinase 12, and heparin-binding epidermal growth factor. Histopathology 69:99–106CrossRefPubMed Da Costa NM, Fialho AD, Proietti CC, da Silva Kataoka MS, Jaeger RG, de Alves-Junior SM, de Jesus Viana Pinheiro J (2016) Role of hypoxia-related proteins in invasion of ameloblastoma cells: crosstalk between NOTCH1, hypoxia-inducible factor 1alpha, a disintegrin and metalloproteinase 12, and heparin-binding epidermal growth factor. Histopathology 69:99–106CrossRefPubMed
25.
Zurück zum Zitat Oral O, Akkoc Y, Bayraktar O, Gozuacik D (2016) Physiological and pathological significance of the molecular cross-talk between autophagy and apoptosis. Histol Histopathol 31:479–498PubMed Oral O, Akkoc Y, Bayraktar O, Gozuacik D (2016) Physiological and pathological significance of the molecular cross-talk between autophagy and apoptosis. Histol Histopathol 31:479–498PubMed
26.
Zurück zum Zitat Shalini S, Dorstyn L, Dawar S, Kumar S (2015) Old, new and emerging functions of caspases. Cell Death Differ 22:526–539CrossRefPubMed Shalini S, Dorstyn L, Dawar S, Kumar S (2015) Old, new and emerging functions of caspases. Cell Death Differ 22:526–539CrossRefPubMed
27.
Zurück zum Zitat Gregoraszczuk EL, Rak-Mardyla A, Rys J, Jakubowicz J, Urbanski K (2015) Effect of chemotherapeutic drugs on caspase-3 activity, as a key biomarker for apoptosis in ovarian tumor cell cultured as monolayer. A pilot study. Iran J Pharm Res 14:1153–1161PubMedPubMedCentral Gregoraszczuk EL, Rak-Mardyla A, Rys J, Jakubowicz J, Urbanski K (2015) Effect of chemotherapeutic drugs on caspase-3 activity, as a key biomarker for apoptosis in ovarian tumor cell cultured as monolayer. A pilot study. Iran J Pharm Res 14:1153–1161PubMedPubMedCentral
28.
Zurück zum Zitat Edelstein CL (2008) Mammalian target of rapamycin and caspase inhibitors in polycystic kidney disease. Clin J Am Soc Nephrol 3:1219–1226CrossRefPubMed Edelstein CL (2008) Mammalian target of rapamycin and caspase inhibitors in polycystic kidney disease. Clin J Am Soc Nephrol 3:1219–1226CrossRefPubMed
29.
Zurück zum Zitat Tao Y, Kim J, Faubel S, Wu JC, Falk SA, Schrier RW, Edelstein CL (2005) Caspase inhibition reduces tubular apoptosis and proliferation and slows disease progression in polycystic kidney disease. Proc Natl Acad Sci U S A 102:6954–6959CrossRefPubMedPubMedCentral Tao Y, Kim J, Faubel S, Wu JC, Falk SA, Schrier RW, Edelstein CL (2005) Caspase inhibition reduces tubular apoptosis and proliferation and slows disease progression in polycystic kidney disease. Proc Natl Acad Sci U S A 102:6954–6959CrossRefPubMedPubMedCentral
30.
Zurück zum Zitat Suzuki H, Tomida A, Tsuruo T (2001) Dephosphorylated hypoxia-inducible factor 1alpha as a mediator of p53-dependent apoptosis during hypoxia. Oncogene 20:5779–5788CrossRefPubMed Suzuki H, Tomida A, Tsuruo T (2001) Dephosphorylated hypoxia-inducible factor 1alpha as a mediator of p53-dependent apoptosis during hypoxia. Oncogene 20:5779–5788CrossRefPubMed
31.
33.
Zurück zum Zitat Mourao RV, Junior EC, Barros Silva PG, Turatti E, Mota MR, Alves AP (2016) Study of the relationship between mononuclear inflammatory infiltrate and ki-67 and basement membrane and extracellular matrix protein expression in radicular cysts. Int Endod 49:447–453CrossRef Mourao RV, Junior EC, Barros Silva PG, Turatti E, Mota MR, Alves AP (2016) Study of the relationship between mononuclear inflammatory infiltrate and ki-67 and basement membrane and extracellular matrix protein expression in radicular cysts. Int Endod 49:447–453CrossRef
34.
Zurück zum Zitat Belibi F, Zafar I, Ravichandran K, Segvic AB, Jani A, Ljubanovic DG, Edelstein CL (2011) Hypoxia-inducible factor-1alpha (HIF-1alpha) and autophagy in polycystic kidney disease (PKD). Am J Physiol Renal Physiol 300:1235–1243CrossRef Belibi F, Zafar I, Ravichandran K, Segvic AB, Jani A, Ljubanovic DG, Edelstein CL (2011) Hypoxia-inducible factor-1alpha (HIF-1alpha) and autophagy in polycystic kidney disease (PKD). Am J Physiol Renal Physiol 300:1235–1243CrossRef
35.
Zurück zum Zitat Bohensky J, Shapiro IM, Leshinsky S, Terkhorn SP, Adams CS, Srinivas V (2007) Hif-1 regulation of chondrocyte apoptosis: induction of the autophagic pathway. Autophagy 3:207–214CrossRefPubMed Bohensky J, Shapiro IM, Leshinsky S, Terkhorn SP, Adams CS, Srinivas V (2007) Hif-1 regulation of chondrocyte apoptosis: induction of the autophagic pathway. Autophagy 3:207–214CrossRefPubMed
36.
Zurück zum Zitat Carmeliet P, Dor Y, Herbert JM, Fukumura D, Brusselmans K, Dewerchin M, Neeman M, Bono F, Abramovitch R, Maxwell P, Koch CJ, Ratcliffe P, Moons L, Jain RK, Collen D, Keshert E (1998) Role of HIF-1alpha in hypoxia-mediated apoptosis, cell proliferation and tumour angiogenesis. Nature 394:485–490CrossRefPubMed Carmeliet P, Dor Y, Herbert JM, Fukumura D, Brusselmans K, Dewerchin M, Neeman M, Bono F, Abramovitch R, Maxwell P, Koch CJ, Ratcliffe P, Moons L, Jain RK, Collen D, Keshert E (1998) Role of HIF-1alpha in hypoxia-mediated apoptosis, cell proliferation and tumour angiogenesis. Nature 394:485–490CrossRefPubMed
37.
Zurück zum Zitat Moritz W, Meier F, Stroka DM, Giuliani M, Kugelmeier P, Nett PC, Lehmann R, Candinas D, Gassmann M, Weber M (2002) Apoptosis in hypoxic human pancreatic islets correlates with HIF-1alpha expression. FASEB J 16:745–747PubMed Moritz W, Meier F, Stroka DM, Giuliani M, Kugelmeier P, Nett PC, Lehmann R, Candinas D, Gassmann M, Weber M (2002) Apoptosis in hypoxic human pancreatic islets correlates with HIF-1alpha expression. FASEB J 16:745–747PubMed
38.
Zurück zum Zitat Chen D, Li M, Luo J, Gu W (2003) Direct interactions between hif-1 alpha and mdm2 modulate p53 function. J Biol Chem 278:13595–13598CrossRefPubMed Chen D, Li M, Luo J, Gu W (2003) Direct interactions between hif-1 alpha and mdm2 modulate p53 function. J Biol Chem 278:13595–13598CrossRefPubMed
39.
Zurück zum Zitat Van Hoecke M, Prigent-Tessier AS, Garnier PE, Bertrand NM, Filomenko R, Bettaieb A, Marie C, Beley AG (2007) Evidence of HIF-1 functional binding activity to caspase-3 promoter after photothrombotic cerebral ischemia. Mol Cell Neurosci 34:40–47CrossRefPubMed Van Hoecke M, Prigent-Tessier AS, Garnier PE, Bertrand NM, Filomenko R, Bettaieb A, Marie C, Beley AG (2007) Evidence of HIF-1 functional binding activity to caspase-3 promoter after photothrombotic cerebral ischemia. Mol Cell Neurosci 34:40–47CrossRefPubMed
40.
Zurück zum Zitat Cho SJ, Teng IF, Zhang M, Yin T, Jung YS, Zhang J, Chen X (2015) Hypoxia-inducible factor 1 alpha is regulated by RBM38, a RNA-binding protein and a p53 family target, via mRNA translation. Oncotarget 6:305–316CrossRefPubMed Cho SJ, Teng IF, Zhang M, Yin T, Jung YS, Zhang J, Chen X (2015) Hypoxia-inducible factor 1 alpha is regulated by RBM38, a RNA-binding protein and a p53 family target, via mRNA translation. Oncotarget 6:305–316CrossRefPubMed
41.
Zurück zum Zitat Gadbail AR, Patil R, Chaudhary M (2012) Co-expression of ki-67 and p53 protein in ameloblastoma and keratocystic odontogenic tumor. Acta Odontol Scand 70:529–535CrossRefPubMed Gadbail AR, Patil R, Chaudhary M (2012) Co-expression of ki-67 and p53 protein in ameloblastoma and keratocystic odontogenic tumor. Acta Odontol Scand 70:529–535CrossRefPubMed
42.
Zurück zum Zitat Nodit L, Barnes L, Childers E, Finkelstein S, Swalsky P, Hunt J (2004) Allelic loss of tumor suppressor genes in ameloblastic tumors. Mod Pathol 17:1062–1067CrossRefPubMed Nodit L, Barnes L, Childers E, Finkelstein S, Swalsky P, Hunt J (2004) Allelic loss of tumor suppressor genes in ameloblastic tumors. Mod Pathol 17:1062–1067CrossRefPubMed
43.
Zurück zum Zitat Buchholz B, Schley G, Faria D, Kroening S, Willam C, Schreiber R, Klanke B, Burzlaff N, Jantsch J, Kunzelmann K, Eckardt KU (2014) Hypoxia-inducible factor-1alpha causes renal cyst expansion through calcium-activated chloride secretion. J Am Soc Nephrol 25:465–474CrossRefPubMed Buchholz B, Schley G, Faria D, Kroening S, Willam C, Schreiber R, Klanke B, Burzlaff N, Jantsch J, Kunzelmann K, Eckardt KU (2014) Hypoxia-inducible factor-1alpha causes renal cyst expansion through calcium-activated chloride secretion. J Am Soc Nephrol 25:465–474CrossRefPubMed
44.
Zurück zum Zitat Casely-Hayford MA, Nicholas SA, Sumbayev VV (2009) Azinomycin epoxide induces activation of apoptosis signal-regulating kinase 1 (ask1) and caspase 3 in a hif-1alpha-independent manner in human leukaemia myeloid macrophages. Eur J Pharmacol 602:262–267CrossRefPubMed Casely-Hayford MA, Nicholas SA, Sumbayev VV (2009) Azinomycin epoxide induces activation of apoptosis signal-regulating kinase 1 (ask1) and caspase 3 in a hif-1alpha-independent manner in human leukaemia myeloid macrophages. Eur J Pharmacol 602:262–267CrossRefPubMed
46.
47.
Zurück zum Zitat Kohl R, Zhou J, Brune B (2006) Reactive oxygen species attenuate nitric-oxide-mediated hypoxia-inducible factor-1alpha stabilization. Free Radic Biol Med 40:1430–1442CrossRefPubMed Kohl R, Zhou J, Brune B (2006) Reactive oxygen species attenuate nitric-oxide-mediated hypoxia-inducible factor-1alpha stabilization. Free Radic Biol Med 40:1430–1442CrossRefPubMed
48.
Zurück zum Zitat Kichi E, Enokiya Y, Muramatsu T, Hashimoto S, Inoue T, Abiko Y, Shimono M (2005) Cell proliferation, apoptosis and apoptosis-related factors in odontogenic keratocysts and in dentigerous cysts. Oral Pathol Med 34:280–286CrossRef Kichi E, Enokiya Y, Muramatsu T, Hashimoto S, Inoue T, Abiko Y, Shimono M (2005) Cell proliferation, apoptosis and apoptosis-related factors in odontogenic keratocysts and in dentigerous cysts. Oral Pathol Med 34:280–286CrossRef
49.
Zurück zum Zitat Metgud R, Gupta K (2013) Expression of cell cycle and apoptosis-related proteins in ameloblastoma and keratocystic odontogenic tumor. Ann Diagn Pathol 17:518–521CrossRefPubMed Metgud R, Gupta K (2013) Expression of cell cycle and apoptosis-related proteins in ameloblastoma and keratocystic odontogenic tumor. Ann Diagn Pathol 17:518–521CrossRefPubMed
50.
Zurück zum Zitat Pinheiro JJ, Freitas VM, Moretti AI, Jorge AG, Jaeger RG (2004) Local invasiveness of ameloblastoma. Role played by matrix metalloproteinases and proliferative activity. Histopathology 45:65–72CrossRefPubMed Pinheiro JJ, Freitas VM, Moretti AI, Jorge AG, Jaeger RG (2004) Local invasiveness of ameloblastoma. Role played by matrix metalloproteinases and proliferative activity. Histopathology 45:65–72CrossRefPubMed
51.
Zurück zum Zitat Siqueira AS, Carvalho MR, Monteiro AC, Freitas VM, Jaeger RG, Pinheiro JJ (2010) Matrix metalloproteinases, timps and growth factors regulating ameloblastoma behaviour. Histopathology 57:128–137CrossRefPubMed Siqueira AS, Carvalho MR, Monteiro AC, Freitas VM, Jaeger RG, Pinheiro JJ (2010) Matrix metalloproteinases, timps and growth factors regulating ameloblastoma behaviour. Histopathology 57:128–137CrossRefPubMed
52.
Zurück zum Zitat Ribeiro AL, Nobre RM, Alves-Junior SM, Kataoka MS, Barroso RF, Jaeger RG, Pinheiro JJ (2012) Matrix metalloproteinases, tissue inhibitors of metalloproteinases, and growth factors regulate the aggressiveness and proliferative activity of keratocystic odontogenic tumors. Oral Surg Oral Med Oral Pathol Oral Radiol 114:487–496CrossRefPubMed Ribeiro AL, Nobre RM, Alves-Junior SM, Kataoka MS, Barroso RF, Jaeger RG, Pinheiro JJ (2012) Matrix metalloproteinases, tissue inhibitors of metalloproteinases, and growth factors regulate the aggressiveness and proliferative activity of keratocystic odontogenic tumors. Oral Surg Oral Med Oral Pathol Oral Radiol 114:487–496CrossRefPubMed
53.
Zurück zum Zitat Ribeiro AL, Nobre RM, Rocha GC, Lobato IH, Alves-Junior SM, Jaeger RG, Pinheiro JJ (2011) Expression of metallothionein in ameloblastoma. A regulatory molecule? J Oral Pathol Med 40:516–519CrossRefPubMed Ribeiro AL, Nobre RM, Rocha GC, Lobato IH, Alves-Junior SM, Jaeger RG, Pinheiro JJ (2011) Expression of metallothionein in ameloblastoma. A regulatory molecule? J Oral Pathol Med 40:516–519CrossRefPubMed
54.
Zurück zum Zitat Ribeiro Ribeiro AL, da Costa NM, de Siqueira AS, Brasil da Silva W, da Silva Kataoka MS, Jaeger RG, Alves-Junior SM, Smith AM, Pinheiro JJ (2016) Keratocystic odontogenic tumor overexpresses invadopodia-related proteins, suggesting invadopodia formation. Oral Surg Oral Med Oral Pathol Oral Radiol 122:500–508CrossRefPubMed Ribeiro Ribeiro AL, da Costa NM, de Siqueira AS, Brasil da Silva W, da Silva Kataoka MS, Jaeger RG, Alves-Junior SM, Smith AM, Pinheiro JJ (2016) Keratocystic odontogenic tumor overexpresses invadopodia-related proteins, suggesting invadopodia formation. Oral Surg Oral Med Oral Pathol Oral Radiol 122:500–508CrossRefPubMed
Metadaten
Titel
Role of HIF-1α and CASPASE-3 in cystogenesis of odontogenic cysts and tumors
verfasst von
Natacha M. M. da Costa
Adriane S. de Siqueira
André L. R. Ribeiro
Maria S. da Silva Kataoka
Ruy G. Jaeger
Sérgio M. de Alves-Júnior
Andrew M. Smith
João de Jesus Viana Pinheiro
Publikationsdatum
25.02.2017
Verlag
Springer Berlin Heidelberg
Erschienen in
Clinical Oral Investigations / Ausgabe 1/2018
Print ISSN: 1432-6981
Elektronische ISSN: 1436-3771
DOI
https://doi.org/10.1007/s00784-017-2090-6

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