Connexin hemichannel induced vascular leak suggests a new paradigm for cancer therapy

FEBS Letters

Volumn 588, Issue 8, 2014, Pages 1365-1371

  Zhang, Jie ^a   O'Carroll, Simon J ^a   Henare, Kimiora ^b   Ching, Lai Ming ^b   Ormonde, Susan ^a   Nicholson, Louise F B ^a   Danesh Meyer, Helen V ^a   Green, Colin R ^a  

^a UNIVERSITY OF AUCKLAND   (New Zealand)

^b UNIVERSITY OF AUCKLAND   (New Zealand)

Author keywords

Cancer drug delivery; Cancer neovascularisation; Cancer treatment; Connexin hemichannel; Gap junction; Microvascular integrity

Indexed keywords

CANCER DRUG DELIVERY; CANCER NEOVASCULARISATION; CANCER TREATMENT; CONNEXIN HEMICHANNEL; GAP JUNCTION; MICROVASCULAR INTEGRITY;

ANGIOGENESIS INHIBITORS; ANIMALS; CONNEXINS; ENDOTHELIUM, VASCULAR; GAP JUNCTIONS; HUMANS; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; PEPTIDES;

EID: 84898874113     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1016/j.febslet.2014.02.003     Document Type: Conference Paper

References (82)

1. J. Folkman Tumor angiogenesis: therapeutic implications N. Engl. J. Med. 285 21 1971 1182 1186
2. A. Iagaru, and S.S. Gambhir Imaging tumor angiogenesis: the road to clinical utility AJR Am. J. Roentgenol. 201 2 2013 W183 W191
3. S.L. Hernandez et al. Notch and VEGF pathways play distinct but complementary roles in tumor angiogenesis Vasc. Cell 5 1 2013 17
4. B.T. Oronsky, S.J. Knox, and J. Scicinski Six degrees of separation: the oxygen effect in the development of radiosensitizers Transl. Oncol. 4 4 2011 189 198
5. D.A. Nelson et al. Hypoxia and defective apoptosis drive genomic instability and tumorigenesis Genes Dev. 18 17 2004 2095 2107 (Pubitemid 39166627)
6. R.K. Jain Normalization of tumor vasculature: an emerging concept in antiangiogenic therapy Science 307 5706 2005 58 62 (Pubitemid 40093472)
7. E.J. Kushner, and V.L. Bautch Building blood vessels in development and disease Curr. Opin. Hematol. 20 3 2013 231 236
8. R.K. Jain Normalizing tumor microenvironment to treat cancer: bench to bedside to biomarkers J. Clin. Oncol. 31 17 2013 2205 2218
9. M.R. Junttila, and F.J. de Sauvage Influence of tumour micro-environment heterogeneity on therapeutic response Nature 501 7467 2013 346 354
10. C.G. Willett et al. Direct evidence that the VEGF-specific antibody bevacizumab has antivascular effects in human rectal cancer Nat. Med. 10 2 2004 145 147 (Pubitemid 38524883)
11. R.J. Young, and M.W. Reed Anti-angiogenic therapy: concept to clinic Microcirculation 19 2 2012 115 125
12. F. Elice, and F. Rodeghiero Side effects of anti-angiogenic drugs Thromb. Res. 129 Suppl. 1 2012 S50 S53
13. D. Li et al. Tumor resistance to anti-VEGF therapy through up-regulation of VEGF-C expression Cancer Lett. 2013 10.1016/j.canlet.2013.12.004 [Epub ahead of print]
14. S. Ananthnarayan et al. Time course of imaging changes of GBM during extended bevacizumab treatment J. Neurooncol. 88 3 2008 339 347
15. M. Cronin et al. Blocking connexin43 expression reduces inflammation and improves functional recovery after spinal cord injury Mol. Cell. Neurosci. 39 2 2008 152 160
16. H.V. Danesh-Meyer et al. Connexin43 antisense oligodeoxynucleotide treatment down-regulates the inflammatory response in an in vitro interphase organotypic culture model of optic nerve ischaemia J. Clin. Neurosci. 15 11 2008 1253 1263
17. R. Mori et al. Acute downregulation of connexin43 at wound sites leads to a reduced inflammatory response, enhanced keratinocyte proliferation and wound fibroblast migration J. Cell Sci. 119 Pt 24 2006 5193 5203 (Pubitemid 46085197)
18. S. Tsuchida et al. Silencing the expression of connexin 43 decreases inflammation and joint destruction in experimental arthritis J. Orthop. Res. 31 4 2013 525 530
19. V. Balasubramaniyan et al. Importance of Connexin-43 based gap junction in cirrhosis and acute-on-chronic liver failure J. Hepatol. 58 6 2013 1194 1200
20. M.V. Frantseva, L. Kokarovtseva, and J.L. Perez Velazquez Ischemia-induced brain damage depends on specific gap-junctional coupling J. Cereb. Blood Flow Metab. 22 4 2002 453 462 (Pubitemid 34273601)
21. J.H. Lin et al. Gap-junction-mediated propagation and amplification of cell injury Nat. Neurosci. 1 6 1998 494 500
22. A. Rawanduzy et al. Effective reduction of infarct volume by gap junction blockade in a rodent model of stroke J. Neurosurg. 87 6 2009 916 920
23. P. Coutinho et al. Limiting burn extension by transient inhibition of Connexin43 expression at the site of injury Br. J. Plast. Surg. 58 5 2005 658 667 (Pubitemid 40903713)
24. C. Qiu et al. Targeting connexin43 expression accelerates the rate of wound repair Curr. Biol. 13 19 2003 1697 1703 (Pubitemid 37216247)
25. M.J. Velardo et al. Patterns of gene expression reveal a temporally orchestrated wound healing response in the injured spinal cord J. Neurosci. 24 39 2004 8562 8576 (Pubitemid 39313779)
26. C.N. Grupcheva et al. Improved corneal wound healing through modulation of gap junction communication using connexin43-specific antisense oligodeoxynucleotides Invest. Ophthalmol. Vis. Sci. 53 3 2012 1130 1138
27. S. Morel, and B.R. Kwak Roles of connexins in atherosclerosis and ischemia-reperfusion injury Curr. Pharm. Biotechnol. 13 1 2012 17 26
28. K.E. Scheckenbach et al. Connexin channel-dependent signaling pathways in inflammation J. Vasc. Res. 48 2 2011 91 103
29. T.M. McIntyre et al. Cell-cell interactions: leukocyte-endothelial interactions Curr. Opin. Hematol. 10 2 2003 150 158 (Pubitemid 36207971)
30. I. Scerri et al. Gap junctional communication does not contribute to the interaction between neutrophils and airway epithelial cells Cell Commun. Adhes. 13 1-2 2006 1 12
31. M.R. DiStasi, and K. Ley Opening the flood-gates: how neutrophil-endothelial interactions regulate permeability Trends Immunol. 30 11 2009 547 556
32. E. Oviedo-Orta, and W. Howard Evans Gap junctions and connexin-mediated communication in the immune system Biochim. Biophys. Acta 1662 1-2 2004 102 112 (Pubitemid 38366516)
33. E.A. Eugenin et al. TNF-alpha plus IFN-gamma induce connexin43 expression and formation of gap junctions between human monocytes/macrophages that enhance physiological responses J. Immunol. 170 3 2003 1320 1328 (Pubitemid 36139499)
34. M.Z. Sarieddine et al. Connexin43 modulates neutrophil recruitment to the lung J. Cell Mol. Med. 13 11-12 2009 4560 4570
35. R.L. Conhaim et al. Bacteremic sepsis disturbs alveolar perfusion distribution in the lungs of rats Crit. Care Med. 36 2 2008 511 517 (Pubitemid 351158627)
36. V. Combes et al. Cerebral malaria: which parasite? Which model? Drug Discov. Today: Dis. Models 2 2 2005 141 147 (Pubitemid 40960355)
37. J. Martini et al. Impairment of functional capillary density but not oxygen delivery in the hamster window chamber during severe experimental malaria Am. J. Pathol. 170 2 2007 505 517 (Pubitemid 47339388)
38. H.C. van der Heyde et al. A unified hypothesis for the genesis of cerebral malaria: sequestration, inflammation and hemostasis leading to microcirculatory dysfunction Trends Parasitol. 22 11 2006 503 508
39. J. Zhang et al. Connexin-Based Therapeutic Approaches to Inflammation in the Central Nervous System E. Oviedo-Orta, B.R. Kwak, W.H. Evans, Connexin Cell Communication Channels 2013 CRC Press
40. S. Vuorisalo, M. Venermo, and M. Lepantalo Treatment of diabetic foot ulcers J. Cardiovasc. Surg. (Torino) 50 3 2009 275 291
41. S. Gist et al. Wound care in the geriatric client Clin. Interv. Aging 4 2009 269 287
42. E. Farkas, and P.G. Luiten Cerebral microvascular pathology in aging and Alzheimer's disease Prog. Neurobiol. 64 6 2001 575 611 (Pubitemid 32304447)
43. J. Guan et al. Vascular degeneration in Parkinson's disease Brain Pathol. 23 2 2013 154 164
44. S. Hunot, and E.C. Hirsch Neuroinflammatory processes in Parkinson's disease Ann. Neurol. 53 Suppl. 3 2003 S49 S58 discussion S58-60
45. L.A. Corvalan et al. Injury of skeletal muscle and specific cytokines induce the expression of gap junction channels in mouse dendritic cells J. Cell Physiol. 211 3 2007 649 660 (Pubitemid 46683033)
46. M. De Bock et al. Connexin channels provide a target to manipulate brain endothelial calcium dynamics and blood-brain barrier permeability J. Cereb. Blood Flow Metab. 31 9 2011 1942 1957
47. K. Nagasawa et al. Possible involvement of gap junctions in the barrier function of tight junctions of brain and lung endothelial cells J. Cell Physiol. 208 1 2006 123 132 (Pubitemid 43848996)
48. M. Faigle et al. ATP release from vascular endothelia occurs across Cx43 hemichannels and is attenuated during hypoxia PLoS One 3 7 2008 e2801
49. H.V. Danesh-Meyer et al. Connexin43 mimetic peptide reduces vascular leak and retinal ganglion cell death following retinal ischaemia Brain 135 Pt 2 2012 506 520
50. M. Krueger et al. Blood-brain barrier breakdown after embolic stroke in rats occurs without ultrastructural evidence for disrupting tight junctions PLoS One 8 2 2013 e56419
51. E.C. Johnson et al. Chronology of optic nerve head and retinal responses to elevated intraocular pressure Invest. Ophthalmol. Vis. Sci. 41 2 2000 431 442 (Pubitemid 30080446)
52. E.C. Johnson et al. Global changes in optic nerve head gene expression after exposure to elevated intraocular pressure in a rat glaucoma model Invest. Ophthalmol. Vis. Sci. 48 7 2007 3161 3177 (Pubitemid 351261161)
53. O. Arend et al. Pathogenetic aspects of the glaucomatous optic neuropathy: fluorescein angiographic findings in patients with primary open angle glaucoma Brain Res. Bull. 62 6 2004 517 524 (Pubitemid 38253037)
54. J.K. Ahn, J.H. Kang, and K.H. Park Correlation between a disc hemorrhage and peripapillary atrophy in glaucoma patients with a unilateral disc hemorrhage J. Glaucoma 13 1 2004 9 14 (Pubitemid 38112347)
55. B.O. Bengtsson, C. Holmin, and C.E.T. Krakau Disc haemorrhage and glaucoma Acta Ophthalmol. 59 1 1981 1 14 (Pubitemid 11191167)
56. D.H. Anderson et al. The pivotal role of the complement system in aging and age-related macular degeneration: hypothesis re-visited Prog. Retin. Eye Res. 29 2 2010 95 112
57. J.Z. Nowak Age-related macular degeneration (AMD): pathogenesis and therapy Pharmacol. Rep. 58 3 2006 353 363 (Pubitemid 44111070)
58. N.J. Coorey et al. The role of glia in retinal vascular disease Clin. Exp. Optom. 95 3 2012 266 281
59. P.T. de Jong Age-related macular degeneration N. Engl. J. Med. 355 14 2006 1474 1485 (Pubitemid 44511562)
60. P.T. Finger et al. Ophthalmic plaque radiotherapy for age-related macular degeneration associated with subretinal neovascularization Am. J. Ophthalmol. 127 2 1999 170 177 (Pubitemid 29072557)
61. D.F. Martin et al. Ranibizumab and bevacizumab for treatment of neovascular age-related macular degeneration: two-year results Ophthalmology 119 7 2012 1388 1398
62. S.F. Abcouwer et al. Effects of ischemic preconditioning and bevacizumab on apoptosis and vascular permeability following retinal ischemia-reperfusion injury Invest. Ophthalmol. Vis. Sci. 51 11 2010 5920 5933
63. C.A. Wilson et al. Blood-retinal barrier breakdown following experimental retinal ischemia and reperfusion Exp. Eye Res. 61 5 1995 547 557
64. L. Zheng et al. Retinal ischemia and reperfusion causes capillary degeneration: similarities to diabetes Invest. Ophthalmol. Vis. Sci. 48 1 2007 361 367 (Pubitemid 47251425)
65. A.P. Quist et al. Physiological role of gap-junctional hemichannels. Extracellular calcium-dependent isosmotic volume regulation J. Cell Biol. 148 5 2000 1063 1074
66. A. Rapisarda, and G. Melillo Role of the VEGF/VEGFR axis in cancer biology and therapy Adv. Cancer Res. 114 2012 237 267
67. D. Tilki et al. Molecular imaging of tumor blood vessels in prostate cancer Anticancer Res. 29 5 2009 1823 1829
68. A. Gosain et al. Exogenous pro-angiogenic stimuli cannot prevent physiologic vessel regression J. Surg. Res. 135 2 2006 218 225 (Pubitemid 44414889)
69. S. Ormonde et al. Regulation of connexin43 gap junction protein triggers vascular recovery and healing in human ocular persistent epithelial defect wounds J. Membr. Biol. 245 7 2012 381 388
70. S.J. O'Carroll et al. Connexin 43 mimetic peptides reduce swelling, astrogliosis, and neuronal cell death after spinal cord injury Cell Commun. Adhes. 15 1 2008 27 42
71. I.F. Tannock The relation between cell proliferation and the vascular system in a transplanted mouse mammary tumour Br. J. Cancer 22 2 1968 258 273
72. I.F. Tannock Population kinetics of carcinoma cells, capillary endothelial cells, and fibroblasts in a transplanted mouse mammary tumor Cancer Res. 30 10 1970 2470 2476
73. S.A. Patil et al. Chromenes: potential new chemotherapeutic agents for cancer Future Med. Chem. 5 14 2013 1647 1660
74. L.B. Harrison et al. Impact of tumor hypoxia and anemia on radiation therapy outcomes Oncologist 7 6 2002 492 508 (Pubitemid 36008998)
75. A.M. Chacko et al. Targeted delivery of antibody-based therapeutic and imaging agents to CNS tumors: crossing the blood-brain barrier divide Expert Opin. Drug Deliv. 10 7 2013 907 926
76. E.M. Thompson et al. Inhibition of SUR1 decreases the vascular permeability of cerebral metastases Neoplasia 15 5 2013 535 543
77. G. Dahl, and R.W. Keane Pannexin: from discovery to bedside in 11+/-4 years? Brain Res. 1487 2012 150 159
78. M.V. Bennett et al. Connexin and pannexin hemichannels in inflammatory responses of glia and neurons Brain Res. 1487 2012 3 15
79. A.W. Lohman et al. Expression of pannexin isoforms in the systemic murine arterial network J. Vasc. Res. 49 5 2012 405 416
80. A. Chandrasekhar et al. Intercellular redistribution of cAMP underlies selective suppression of cancer cell growth by connexin26 PLoS One 8 12 2013 e82335
81. T. Okamoto et al. Endothelial connexin32 enhances angiogenesis by positively regulating tube formation and cell migration Exp. Cell Res. 321 2 2014 133 141
82. T. Donnem et al. Vessel co-option in primary human tumors and metastases: an obstacle to effective anti-angiogenic treatment? Cancer Med. 2 4 2013 427 436