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Tunneling Nanotube (TNT) Mediated Intercellular Crosstalk and Autophagy in Hypoxia-Induced Mesenchymal Stem Cells

Yıl 2025, Cilt: 8 Sayı: 2, 435 - 443

Gizem İlter Aktaş , Şeyma Kipel , Leyla Didem Kozaci , Habibe Meltem Özgüner

https://doi.org/10.34248/bsengineering.1606557

Öz

Intercellular communication is a critical process and multicellular organisms rely on communication networks to coordinate and maintain physiological functions. Tunneling nanotubes (TNTs) defined as a novel cell to cell communication mechanism and characterized by F-actin. TNTs allow the rapid exchange of cellular cargos including organelles, vesicles, molecules etc. Hypoxia plays an essential role in stem cell functions and also a known stimulus of autophagy. Autophagy and Wnt/β-catenin signalling pathways have important roles during essential cellular processes like tissue homeostasis. This study was aimed to investigate the effect of hypoxia on autophagy, Wnt/β-catenin signalling and the formation of TNTs in bone marrow mesenchymal stem cells (BM-MSCs). Western blotting was applied for HIF-1α protein expression. Immunolabeling was applied to investigate LC3B, p62 and β-catenin protein expressions. Immunofluorescence staining was assessed to evaluate TNT formations and HIF-1α protein. HIF-1α protein expression was significantly increased in CoCl2 induced hypoxic BM-MSCs compared to the normoxia. As a result of the immunofluorescence staining, HIF-1α was positively stained in the cell nuclei of hypoxic BM-MSCs. Number and lengths of TNT formations was increased in hypoxic BM-MSCs compared to the normoxia. Also, we showed that hypoxia upregulates LC3B and downregulates p62 expression. In conclusion, our study indicates that TNT-mediated intercellular communication increases under the hypoxia in BM-MSCs and hypoxic microenvironment may be a significant factor for stem cell functions. Our findings may also draw attention to a possible TNT-mediated crosstalk for autophagy and Wnt/β-catenin signalling mechanism between distant cells.

Anahtar Kelimeler

Autophagy Hypoxia Intercellular communication Mesenchymal stem cell Tunneling nanotubes Wnt signalling

Etik Beyan

Ethics committee approval was not required for this study because of there was no study on animals or humans.

Kaynakça

  • Arthur A, Gronthos S. 2020. Clinical application of bone marrow mesenchymal stem/stromal cells to repair skeletal tissue. Inter J Molec Sci, 21(24): 9759.
  • Austefjord M, Gerdes H, Wang X. 2014. Tunneling nanotubes: Diversity in morphology and structure. Commun Integr Biol 7(1): 1-11.
  • Baker N, Boyette L, Tuan R. 2015. Characterization of bone marrow-derived mesenchymal stem cells in aging. Bone, 70: 37-47.
  • Bhandi S, Kahtani A, Mashyakhy M, Alsofi L, Maganur P, Vishwanathaiah S, Testarelli L, Giudice A, Mehta D, Vyas N, Patil V, Raj A, Patil S. 2021. Modulation of the dental pulp stem cell secretory profile by hypoxia induction using cobalt chloride. J Pers Med, 11(4): 247.
  • Bornes T, Adesida A, Jomha N. 2014. Mesenchymal stem cells in the treatment of traumatic articular cartilage defects: a comprehensive review. Arthritis Res Ther, 16(5): 1-19.
  • Buravkova L, Andreeva E, Grigoriev A. 2012. The impact of oxygen in physiological regulation of human multipotent mesenchymal cell functions. Fiziol Cheloveka, 38 (4): 121-130.
  • Chen Y, Zhao Q, Yang X, Yu X, Yu D, Zhao W. 2019. Effects of cobalt chloride on the stem cell marker expression and osteogenic differentiation of stem cells from human exfoliated deciduous teeth. Cell Stress and Chaperones, 24(3): 527-538.
  • Ciavarella C, Fittipaldi S, Pasquinelli G. 2016. CoCl2 Administration to vascular MSC cultures as an in vitro hypoxic system to study stem cell survival and angiogenesis. Methods Mol Biol, 2016: 309-317.
  • Desir S, Dickson E, Vogel R, Thayanithy V, Wong P, Teoh, D, Geller M, Steer C, Subramanian S, Lou E. 2016. Tunneling nanotube formation is stimulated by hypoxia in ovarian cancer cells. Oncotarget, 7(28): 43150-43161.
  • Di Mattia M, Mauro A, Citeroni M, Dufrusine B, Peserico A, Russo V, Berardinelli P, Dainese E, Cimini A, Barboni B. 2021. Insight into hypoxia stemness control. Cells, 10(8): 2161.
  • Formicola B, D'Aloia A, Dal Magro R, Stucchi S, Rigolio R, Ceriani M, Re F. 2019. Differential exchange of multifunctional liposomes between glioblastoma cells and healthy astrocytes via tunneling nanotubes. Front Bioeng Biotechnol, 7: 403.
  • Gerdes H, Carvalho R. 2008. Intercellular transfer mediated by tunneling nanotubes. Curr Opin Cell Biol, 20(4): 470-475.
  • Gerdes H, Rustom A, Wang, X. 2013. Tunneling nanotubes, an emerging intercellular communication route in development. Mech Dev, 130(6-8): 381-387.
  • Gleadle J, Ratcliffe P. 1998. Hypoxia and the regulation of gene expression. Mol Med Today, 4(3): 122-129.
  • Gurke S, Barroso J, Gerdes H. 2008. The art of cellular communication: tunneling nanotubes bridge the divide. Histochem Cell Biol, 129(5): 539-550.
  • Jaakkola P, Mursiheimo, J. 2009. p62 degradation by autophagy: another way for cancer cells to survive under hypoxia. Autophagy, 5(3): 410-412.
  • Jackson M, Morrison T, Doherty D, McAuley D, Matthay M, Kissenpfennig A, O’Kane C, Krasnodembskaya, A. 2016. Mitochondrial transfer via tunneling nanotubes is an important mechanism by which mesenchymal stem cells enhance macrophage phagocytosis in the in vitro and in vivo models of ARDS. Stem Cells, 34(8): 2210-2223.
  • Kato K, Nguyen K, Decker W, Silkwood H, Eck S, Hernandez, J, Garcia J, Han, D. 2022. Tunneling nanotube formation promotes survival against 5‐fluorouracil in MCF‐7 breast cancer cells. FEBS Open Bio, 12(1): 203-210.
  • Kolba D, Dudka W, Zaręba-Kozioł M, Kominek A, Ronchi P, Turos L, Chroscicki P, Wlodarczyk J, Schwab Y, Klejman A, Cysewski D, Srpan K, Davis D, Piwocka K. 2019. Tunneling nanotube- mediated intercellular vesicle and protein transfer in the stroma- provided imatinib resistance in chronic myeloid leukemia cells. Cell Death Disease, 10(11): 817.
  • Laksana K, Sooampon S, Pavasant, P, Sriarj, W. 2017. Cobalt chloride enhances the stemness of human dental pulp cells. J Endod, 43(5): 760-765.
  • Liu L, Simon C. 2004. Regulation of transcription and translation by hypoxia. Cancer Biol Ther, 3(6): 492-497.
  • Liu L, Yu Q, Fu S, Wang B, Hu K, Wang L, Hu Y, Xu Y, Yu X, Huang H. 2018. CXCR4 antagonist AMD3100 promotes mesenchymal stem cell mobilization in rats preconditioned with the hypoxia-mimicking agent cobalt chloride. Stem Cells Develop, 27(7): 466-478.
  • Lorzadeh S, Kohan L, Ghavami S, Azarpira N. 2021. Autophagy and the Wnt signaling pathway: A focus on Wnt/β catenin signaling. Biochim Biophys Acta Mol Cell Res, 1868(3): 118926.
  • Mitani T, Minami M, Harada N, Ashida H, Yamaji R. 2015. Autophagic degradation of the androgen receptor mediated by increased phosphorylation of p62 suppresses apoptosis in hypoxia. Cell Signal, 27(10): 1994-2001.
  • Mittelbrunn M, Sánchez-Madrid, F. 2012. Intercellular communication: diverse structures for exchange of genetic information. Nat Rev Mol Cell Biol, 13(5): 328-335.
  • Monaci S, Aldinucci C, Rossi D, Giuntini G, Filippi I, Ulivieri C, Marotta G, Sozzani S, Carraro F, Naldini A. 2020. Hypoxia shapes autophagy in LPS- activated dendritic cells. Front Immunol, 11: 573646.
  • Murray L, Krasnodembskaya A. 2019. Concise review: intercellular communication via organelle transfer in the biology and therapeutic applications of stem cells. Stem Cells, 37(1): 14-25.
  • Nugraha A, ,Ihsan I, Dinaryanti A, Hendrianto E, Susilowati H, Prasetyo E, Rantam F. A. 2021. Cobalt (II) chloride in enhancing hypoxia inducible factor-1a expression of gingival derived mesenchymal stem cells in vitro. Res J Pharmcy Technol, 14(5): 2639-2642.
  • Petherick K, Williams A, Lane J, Ordóñez‐Morán P, Huelsken J, Collard T, Smartt H, Batson J, Malik K, Paraskeva C, Greenhough A. 2013. Autolysosomal β‐catenin degradation regulates Wnt‐ autophagy‐p62 crosstalk. EMBO J, 32(13): 1903-1916.
  • Roehlecke C, Schmidt M. 2020. Tunneling nanotubes and tumor microtubes in cancer. Cancers, 12(4): 857.
  • Rustom A, Saffrich R, Markovic I, Walther P, Gerdes H. 2004. Nanotubular highways for intercellular organelle transport. Science, 303(5660): 1007-1010.
  • Simon M, Keith B. 2008. The role of oxygen availability in embryonic development and stem cell function. Nat Rev Mol Cell Biol, 9(4): 285-296.
  • Soundara T, Gugliandolo A, Bramanti P, Mazzon E. 2020. Tunneling nanotubes-mediated protection of mesenchymal stem cells: an update from preclinical studies. Int J Mol Sci, 21(10): 3481.
  • Sowinski S, Jolly C, Berninghausen O, Purbhoo A, Chauveau A, Köhler K, Oddos S, Eissmann P, Brodsky F, Hopkins C, Onfelt B, Sattentau Q, Davis D. 2008. Membrane nanotubes physically connect T cells over long distances presenting a novel route for HIV-1 transmission. Nat Cell Biol, 10(2): 211-219.
  • Teti G, Focaroli S, Salvatore V, Mazzotti E, Ingra L, Mazzotti A, Falconi M. 2018. The hypoxia-mimetic agent cobalt chloride differently affects human mesenchymal stem cells in their chondrogenic potential. Stem Cells Int, 13: 3237253.
  • Thayanithy V, Dickson E, Steer C, Subramanian S, Lou E. 2014. Tumor-stromal cross talk: direct cell-to-cell transfer of oncogenic microRNAs via tunneling nanotubes. Transl Res, 164(5): 359-365.
  • Wu J, Niu J, Li X, Li Y, Wang X, Lin, J, Zhang F. 2014. Hypoxia induces autophagy of bone marrow-derived mesenchymal stem cells via activation of ERK1/2. Cell Physiol Biochem, 33(5): 1467-1474.
  • Xu W, Zhou W, Cheng M, Wang J, Liu Z, He S, Luo X, Huang W, Chen T, Yan W, Xiao J. 2017. Hypoxia activates Wnt/β-catenin signaling by regulating the expression of BCL9 in human hepatocellular carcinoma. Sci Rep, 7(1): 40446.
  • Yoo H, Moon Y, Kim M. 2016. Effects of CoCl2 on multi- lineage differentiation of C3H/10T1/2 mesenchymal stem cells. Korean J Physiol Pharmacol, 20(1): 53.
  • Yu X, Lu C, Liu H, Rao S, Cai J, Liu S, Kriegel A, Greene A, Liang M, Ding, X. 2013. Hypoxic preconditioning with cobalt of bone marrow mesenchymal stem cells improves cell migration and enhances therapy for treatment of ischemic acute kidney injury. Plos One, 8(5): e62703.
  • Zhang J, Whitehead J, Liu Y, Yang Q, Leach J, Liu G. 2018. Direct observation of tunneling nanotubes within human mesenchymal stem cell spheroids. J Phys Chem B, 122(43): 9920-9926.
  • Zurzolo C. 2021. Tunneling nanotubes: Reshaping connectivity. Curr Opin Cell Biol, 71: 139-147.

Tunneling Nanotube (TNT) Mediated Intercellular Crosstalk and Autophagy in Hypoxia-Induced Mesenchymal Stem Cells

Yıl 2025, Cilt: 8 Sayı: 2, 435 - 443

Gizem İlter Aktaş , Şeyma Kipel , Leyla Didem Kozaci , Habibe Meltem Özgüner

https://doi.org/10.34248/bsengineering.1606557

Öz

Intercellular communication is a critical process and multicellular organisms rely on communication networks to coordinate and maintain physiological functions. Tunneling nanotubes (TNTs) defined as a novel cell to cell communication mechanism and characterized by F-actin. TNTs allow the rapid exchange of cellular cargos including organelles, vesicles, molecules etc. Hypoxia plays an essential role in stem cell functions and also a known stimulus of autophagy. Autophagy and Wnt/β-catenin signalling pathways have important roles during essential cellular processes like tissue homeostasis. This study was aimed to investigate the effect of hypoxia on autophagy, Wnt/β-catenin signalling and the formation of TNTs in bone marrow mesenchymal stem cells (BM-MSCs). Western blotting was applied for HIF-1α protein expression. Immunolabeling was applied to investigate LC3B, p62 and β-catenin protein expressions. Immunofluorescence staining was assessed to evaluate TNT formations and HIF-1α protein. HIF-1α protein expression was significantly increased in CoCl2 induced hypoxic BM-MSCs compared to the normoxia. As a result of the immunofluorescence staining, HIF-1α was positively stained in the cell nuclei of hypoxic BM-MSCs. Number and lengths of TNT formations was increased in hypoxic BM-MSCs compared to the normoxia. Also, we showed that hypoxia upregulates LC3B and downregulates p62 expression. In conclusion, our study indicates that TNT-mediated intercellular communication increases under the hypoxia in BM-MSCs and hypoxic microenvironment may be a significant factor for stem cell functions. Our findings may also draw attention to a possible TNT-mediated crosstalk for autophagy and Wnt/β-catenin signalling mechanism between distant cells.

Anahtar Kelimeler

Autophagy Hypoxia Intercellular communication Mesenchymal stem cell Tunneling nanotubes Wnt signalling

Etik Beyan

Ethics committee approval was not required for this study because of there was no study on animals or humans.

Kaynakça

  • Arthur A, Gronthos S. 2020. Clinical application of bone marrow mesenchymal stem/stromal cells to repair skeletal tissue. Inter J Molec Sci, 21(24): 9759.
  • Austefjord M, Gerdes H, Wang X. 2014. Tunneling nanotubes: Diversity in morphology and structure. Commun Integr Biol 7(1): 1-11.
  • Baker N, Boyette L, Tuan R. 2015. Characterization of bone marrow-derived mesenchymal stem cells in aging. Bone, 70: 37-47.
  • Bhandi S, Kahtani A, Mashyakhy M, Alsofi L, Maganur P, Vishwanathaiah S, Testarelli L, Giudice A, Mehta D, Vyas N, Patil V, Raj A, Patil S. 2021. Modulation of the dental pulp stem cell secretory profile by hypoxia induction using cobalt chloride. J Pers Med, 11(4): 247.
  • Bornes T, Adesida A, Jomha N. 2014. Mesenchymal stem cells in the treatment of traumatic articular cartilage defects: a comprehensive review. Arthritis Res Ther, 16(5): 1-19.
  • Buravkova L, Andreeva E, Grigoriev A. 2012. The impact of oxygen in physiological regulation of human multipotent mesenchymal cell functions. Fiziol Cheloveka, 38 (4): 121-130.
  • Chen Y, Zhao Q, Yang X, Yu X, Yu D, Zhao W. 2019. Effects of cobalt chloride on the stem cell marker expression and osteogenic differentiation of stem cells from human exfoliated deciduous teeth. Cell Stress and Chaperones, 24(3): 527-538.
  • Ciavarella C, Fittipaldi S, Pasquinelli G. 2016. CoCl2 Administration to vascular MSC cultures as an in vitro hypoxic system to study stem cell survival and angiogenesis. Methods Mol Biol, 2016: 309-317.
  • Desir S, Dickson E, Vogel R, Thayanithy V, Wong P, Teoh, D, Geller M, Steer C, Subramanian S, Lou E. 2016. Tunneling nanotube formation is stimulated by hypoxia in ovarian cancer cells. Oncotarget, 7(28): 43150-43161.
  • Di Mattia M, Mauro A, Citeroni M, Dufrusine B, Peserico A, Russo V, Berardinelli P, Dainese E, Cimini A, Barboni B. 2021. Insight into hypoxia stemness control. Cells, 10(8): 2161.
  • Formicola B, D'Aloia A, Dal Magro R, Stucchi S, Rigolio R, Ceriani M, Re F. 2019. Differential exchange of multifunctional liposomes between glioblastoma cells and healthy astrocytes via tunneling nanotubes. Front Bioeng Biotechnol, 7: 403.
  • Gerdes H, Carvalho R. 2008. Intercellular transfer mediated by tunneling nanotubes. Curr Opin Cell Biol, 20(4): 470-475.
  • Gerdes H, Rustom A, Wang, X. 2013. Tunneling nanotubes, an emerging intercellular communication route in development. Mech Dev, 130(6-8): 381-387.
  • Gleadle J, Ratcliffe P. 1998. Hypoxia and the regulation of gene expression. Mol Med Today, 4(3): 122-129.
  • Gurke S, Barroso J, Gerdes H. 2008. The art of cellular communication: tunneling nanotubes bridge the divide. Histochem Cell Biol, 129(5): 539-550.
  • Jaakkola P, Mursiheimo, J. 2009. p62 degradation by autophagy: another way for cancer cells to survive under hypoxia. Autophagy, 5(3): 410-412.
  • Jackson M, Morrison T, Doherty D, McAuley D, Matthay M, Kissenpfennig A, O’Kane C, Krasnodembskaya, A. 2016. Mitochondrial transfer via tunneling nanotubes is an important mechanism by which mesenchymal stem cells enhance macrophage phagocytosis in the in vitro and in vivo models of ARDS. Stem Cells, 34(8): 2210-2223.
  • Kato K, Nguyen K, Decker W, Silkwood H, Eck S, Hernandez, J, Garcia J, Han, D. 2022. Tunneling nanotube formation promotes survival against 5‐fluorouracil in MCF‐7 breast cancer cells. FEBS Open Bio, 12(1): 203-210.
  • Kolba D, Dudka W, Zaręba-Kozioł M, Kominek A, Ronchi P, Turos L, Chroscicki P, Wlodarczyk J, Schwab Y, Klejman A, Cysewski D, Srpan K, Davis D, Piwocka K. 2019. Tunneling nanotube- mediated intercellular vesicle and protein transfer in the stroma- provided imatinib resistance in chronic myeloid leukemia cells. Cell Death Disease, 10(11): 817.
  • Laksana K, Sooampon S, Pavasant, P, Sriarj, W. 2017. Cobalt chloride enhances the stemness of human dental pulp cells. J Endod, 43(5): 760-765.
  • Liu L, Simon C. 2004. Regulation of transcription and translation by hypoxia. Cancer Biol Ther, 3(6): 492-497.
  • Liu L, Yu Q, Fu S, Wang B, Hu K, Wang L, Hu Y, Xu Y, Yu X, Huang H. 2018. CXCR4 antagonist AMD3100 promotes mesenchymal stem cell mobilization in rats preconditioned with the hypoxia-mimicking agent cobalt chloride. Stem Cells Develop, 27(7): 466-478.
  • Lorzadeh S, Kohan L, Ghavami S, Azarpira N. 2021. Autophagy and the Wnt signaling pathway: A focus on Wnt/β catenin signaling. Biochim Biophys Acta Mol Cell Res, 1868(3): 118926.
  • Mitani T, Minami M, Harada N, Ashida H, Yamaji R. 2015. Autophagic degradation of the androgen receptor mediated by increased phosphorylation of p62 suppresses apoptosis in hypoxia. Cell Signal, 27(10): 1994-2001.
  • Mittelbrunn M, Sánchez-Madrid, F. 2012. Intercellular communication: diverse structures for exchange of genetic information. Nat Rev Mol Cell Biol, 13(5): 328-335.
  • Monaci S, Aldinucci C, Rossi D, Giuntini G, Filippi I, Ulivieri C, Marotta G, Sozzani S, Carraro F, Naldini A. 2020. Hypoxia shapes autophagy in LPS- activated dendritic cells. Front Immunol, 11: 573646.
  • Murray L, Krasnodembskaya A. 2019. Concise review: intercellular communication via organelle transfer in the biology and therapeutic applications of stem cells. Stem Cells, 37(1): 14-25.
  • Nugraha A, ,Ihsan I, Dinaryanti A, Hendrianto E, Susilowati H, Prasetyo E, Rantam F. A. 2021. Cobalt (II) chloride in enhancing hypoxia inducible factor-1a expression of gingival derived mesenchymal stem cells in vitro. Res J Pharmcy Technol, 14(5): 2639-2642.
  • Petherick K, Williams A, Lane J, Ordóñez‐Morán P, Huelsken J, Collard T, Smartt H, Batson J, Malik K, Paraskeva C, Greenhough A. 2013. Autolysosomal β‐catenin degradation regulates Wnt‐ autophagy‐p62 crosstalk. EMBO J, 32(13): 1903-1916.
  • Roehlecke C, Schmidt M. 2020. Tunneling nanotubes and tumor microtubes in cancer. Cancers, 12(4): 857.
  • Rustom A, Saffrich R, Markovic I, Walther P, Gerdes H. 2004. Nanotubular highways for intercellular organelle transport. Science, 303(5660): 1007-1010.
  • Simon M, Keith B. 2008. The role of oxygen availability in embryonic development and stem cell function. Nat Rev Mol Cell Biol, 9(4): 285-296.
  • Soundara T, Gugliandolo A, Bramanti P, Mazzon E. 2020. Tunneling nanotubes-mediated protection of mesenchymal stem cells: an update from preclinical studies. Int J Mol Sci, 21(10): 3481.
  • Sowinski S, Jolly C, Berninghausen O, Purbhoo A, Chauveau A, Köhler K, Oddos S, Eissmann P, Brodsky F, Hopkins C, Onfelt B, Sattentau Q, Davis D. 2008. Membrane nanotubes physically connect T cells over long distances presenting a novel route for HIV-1 transmission. Nat Cell Biol, 10(2): 211-219.
  • Teti G, Focaroli S, Salvatore V, Mazzotti E, Ingra L, Mazzotti A, Falconi M. 2018. The hypoxia-mimetic agent cobalt chloride differently affects human mesenchymal stem cells in their chondrogenic potential. Stem Cells Int, 13: 3237253.
  • Thayanithy V, Dickson E, Steer C, Subramanian S, Lou E. 2014. Tumor-stromal cross talk: direct cell-to-cell transfer of oncogenic microRNAs via tunneling nanotubes. Transl Res, 164(5): 359-365.
  • Wu J, Niu J, Li X, Li Y, Wang X, Lin, J, Zhang F. 2014. Hypoxia induces autophagy of bone marrow-derived mesenchymal stem cells via activation of ERK1/2. Cell Physiol Biochem, 33(5): 1467-1474.
  • Xu W, Zhou W, Cheng M, Wang J, Liu Z, He S, Luo X, Huang W, Chen T, Yan W, Xiao J. 2017. Hypoxia activates Wnt/β-catenin signaling by regulating the expression of BCL9 in human hepatocellular carcinoma. Sci Rep, 7(1): 40446.
  • Yoo H, Moon Y, Kim M. 2016. Effects of CoCl2 on multi- lineage differentiation of C3H/10T1/2 mesenchymal stem cells. Korean J Physiol Pharmacol, 20(1): 53.
  • Yu X, Lu C, Liu H, Rao S, Cai J, Liu S, Kriegel A, Greene A, Liang M, Ding, X. 2013. Hypoxic preconditioning with cobalt of bone marrow mesenchymal stem cells improves cell migration and enhances therapy for treatment of ischemic acute kidney injury. Plos One, 8(5): e62703.
  • Zhang J, Whitehead J, Liu Y, Yang Q, Leach J, Liu G. 2018. Direct observation of tunneling nanotubes within human mesenchymal stem cell spheroids. J Phys Chem B, 122(43): 9920-9926.
  • Zurzolo C. 2021. Tunneling nanotubes: Reshaping connectivity. Curr Opin Cell Biol, 71: 139-147.
Toplam 42 adet kaynakça vardır.

Ayrıntılar

Birincil Dil İngilizce
Konular Genetik (Diğer)
Bölüm Research Articles
Yazarlar

Gizem İlter Aktaş 0000-0003-3805-8446

Şeyma Kipel 0000-0002-4176-5136

Leyla Didem Kozaci 0000-0001-5422-1640

Habibe Meltem Özgüner 0000-0003-0364-5907

Yayımlanma Tarihi
Gönderilme Tarihi 26 Aralık 2024
Kabul Tarihi 2 Şubat 2025
Yayımlandığı Sayı Yıl 2025 Cilt: 8 Sayı: 2

Kaynak Göster

APA İlter Aktaş, G., Kipel, Ş., Kozaci, L. D., Özgüner, H. M. (t.y.). Tunneling Nanotube (TNT) Mediated Intercellular Crosstalk and Autophagy in Hypoxia-Induced Mesenchymal Stem Cells. Black Sea Journal of Engineering and Science, 8(2), 435-443. https://doi.org/10.34248/bsengineering.1606557
AMA İlter Aktaş G, Kipel Ş, Kozaci LD, Özgüner HM. Tunneling Nanotube (TNT) Mediated Intercellular Crosstalk and Autophagy in Hypoxia-Induced Mesenchymal Stem Cells. BSJ Eng. Sci. 8(2):435-443. doi:10.34248/bsengineering.1606557
Chicago İlter Aktaş, Gizem, Şeyma Kipel, Leyla Didem Kozaci, ve Habibe Meltem Özgüner. “Tunneling Nanotube (TNT) Mediated Intercellular Crosstalk and Autophagy in Hypoxia-Induced Mesenchymal Stem Cells”. Black Sea Journal of Engineering and Science 8, sy. 2 t.y.: 435-43. https://doi.org/10.34248/bsengineering.1606557.
EndNote İlter Aktaş G, Kipel Ş, Kozaci LD, Özgüner HM Tunneling Nanotube (TNT) Mediated Intercellular Crosstalk and Autophagy in Hypoxia-Induced Mesenchymal Stem Cells. Black Sea Journal of Engineering and Science 8 2 435–443.
IEEE G. İlter Aktaş, Ş. Kipel, L. D. Kozaci, ve H. M. Özgüner, “Tunneling Nanotube (TNT) Mediated Intercellular Crosstalk and Autophagy in Hypoxia-Induced Mesenchymal Stem Cells”, BSJ Eng. Sci., c. 8, sy. 2, ss. 435–443, doi: 10.34248/bsengineering.1606557.
ISNAD İlter Aktaş, Gizem vd. “Tunneling Nanotube (TNT) Mediated Intercellular Crosstalk and Autophagy in Hypoxia-Induced Mesenchymal Stem Cells”. Black Sea Journal of Engineering and Science 8/2 (t.y.), 435-443. https://doi.org/10.34248/bsengineering.1606557.
JAMA İlter Aktaş G, Kipel Ş, Kozaci LD, Özgüner HM. Tunneling Nanotube (TNT) Mediated Intercellular Crosstalk and Autophagy in Hypoxia-Induced Mesenchymal Stem Cells. BSJ Eng. Sci.;8:435–443.
MLA İlter Aktaş, Gizem vd. “Tunneling Nanotube (TNT) Mediated Intercellular Crosstalk and Autophagy in Hypoxia-Induced Mesenchymal Stem Cells”. Black Sea Journal of Engineering and Science, c. 8, sy. 2, ss. 435-43, doi:10.34248/bsengineering.1606557.
Vancouver İlter Aktaş G, Kipel Ş, Kozaci LD, Özgüner HM. Tunneling Nanotube (TNT) Mediated Intercellular Crosstalk and Autophagy in Hypoxia-Induced Mesenchymal Stem Cells. BSJ Eng. Sci. 8(2):435-43.
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