A novel family of fluorescent hypoxia sensors reveal strong heterogeneity in tumor hypoxia at the cellular level

EMBO Journal

Volumn 35, Issue 1, 2016, Pages 102-113

  Erapaneedi, Raghu ^a,b   Belousov, Vsevolod V ^c   Schäfers, Michael ^b,d   Kiefer, Friedemann ^a,b  

^a MAX PLANCK INSTITUTE FOR MOLECULAR BIOMEDICINE   (Germany)

^b Cells in Motion CiM ^*  (Germany)

^c SHEMYAKIN OVCHINNIKOV INSTITUTE OF BIOORGANIC CHEMISTRY   (Russian Federation)

^d INST OF REPRO MED OF THE UNIV   (Germany)

Author keywords

fluorescent protein; hypoxia; microscopy; sensor; UnaG

Indexed keywords

FLUORESCENT DYE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; OXYGEN; RECOMBINANT PROTEIN; UNAG MORANGE FUSION PROTEIN; UNCLASSIFIED DRUG; PHOTOPROTEIN; VASCULOTROPIN A; VEGFA PROTEIN, HUMAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD VESSEL; CELL HETEROGENEITY; CELL HYPOXIA; CELL MIGRATION; CONTROLLED STUDY; FEMALE; FLUORESCENCE; GLIOBLASTOMA; GLIOMA CELL LINE; HUMAN; HUMAN CELL; HYPOXIA; HYPOXIC CELL; IN VIVO STUDY; MALE; MALIGNANT NEOPLASTIC DISEASE; MOUSE; NONHUMAN; ONCOGENESIS AND MALIGNANT TRANSFORMATION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN STABILITY; REOXYGENATION; TRANSCRIPTION INITIATION; TUMOR HYPOXIA; TUMOR MICROENVIRONMENT; ANIMAL; CYTOMEGALOVIRUS; EEL; ENHANCER REGION; FLUORESCENCE MICROSCOPY; GENE FUSION; GENETIC PROCEDURES; GENETICS; NEOPLASM; PATHOLOGY; PROCEDURES; PROMOTER REGION; REPORTER GENE;

ANIMALS; ARTIFICIAL GENE FUSION; BIOSENSING TECHNIQUES; CYTOMEGALOVIRUS; EELS; ENHANCER ELEMENTS, GENETIC; GENES, REPORTER; HUMANS; HYPOXIA; LUMINESCENT PROTEINS; MICROSCOPY, FLUORESCENCE; NEOPLASMS; PROMOTER REGIONS, GENETIC; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84955375766     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.15252/embj.201592775     Document Type: Article

References (49)

1. Apte S, Chin FT, Graves EE, (2011) Molecular Imaging of Hypoxia: strategies for Probe Design and Application. Curr Org Synth 8: 593-603
2. Baumann BC, Dorsey JF, Benci JL, Joh DY, Kao GD, (2012) Stereotactic intracranial implantation and in vivo bioluminescent imaging of tumor xenografts in a mouse model system of glioblastoma multiforme. J Vis Exp 67: 4089
3. Bussink J, Kaanders JH, van der Kogel AJ, (2003) Tumor hypoxia at the micro-regional level: clinical relevance and predictive value of exogenous and endogenous hypoxic cell markers. Radiother Oncol 67: 3-15
4. Cao Y, Li CY, Moeller BJ, Yu D, Zhao Y, Dreher MR, Shan S, Dewhirst MW, (2005) Observation of incipient tumor angiogenesis that is independent of hypoxia and hypoxia inducible factor-1 activation. Cancer Res 65: 5498-5505
5. 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: 485-490
6. Cecic I, Chan DA, Sutphin PD, Ray P, Gambhir SS, Giaccia AJ, Graves EE, (2007) Oxygen sensitivity of reporter genes: implications for preclinical imaging of tumor hypoxia. Mol Imaging 6: 219-228
7. Chan DA, Giaccia AJ, (2007) Hypoxia, gene expression, and metastasis. Cancer Metastasis Rev 26: 333-339
8. Chan DA, Sutphin PD, Yen SE, Giaccia AJ, (2005) Coordinate regulation of the oxygen-dependent degradation domains of hypoxia-inducible factor 1 alpha. Mol Cell Biol 25: 6415-6426
9. Cho EA, Song HK, Lee SH, Chung BH, Lim HM, Lee MK, (2013) Differential in vitro and cellular effects of iron chelators for hypoxia inducible factor hydroxylases. J Cell Biochem 114: 864-873
10. Coralli C, Cemazar M, Kanthou C, Tozer GM, Dachs GU, (2001) Limitations of the reporter green fluorescent protein under simulated tumor conditions. Cancer Res 61: 4784-4790
11. Cui L, Zhong Y, Zhu W, Xu Y, Du Q, Wang X, Qian X, Xiao Y, (2011) A new prodrug-derived ratiometric fluorescent probe for hypoxia: high selectivity of nitroreductase and imaging in tumor cell. Org Lett 13: 928-931
12. Fandrey J, Gorr TA, Gassmann M, (2006) Regulating cellular oxygen sensing by hydroxylation. Cardiovasc Res 71: 642-651
13. Fomicheva EV, Turner II, Edwards TG, Hoff J, Arden E, D'Alecy LG, Metzger JM, (2008) Double oxygen-sensing vector system for robust hypoxia/ischemia-regulated gene induction in cardiac muscle in vitro and in vivo. Mol Ther 16: 1594-1601
14. Friedl P, Zanker KS, Brocker EB, (1998) Cell migration strategies in 3-D extracellular matrix: differences in morphology, cell matrix interactions, and integrin function. Microsc Res Tech 43: 369-378
15. Fujiwara S, Nakagawa K, Harada H, Nagato S, Furukawa K, Teraoka M, Seno T, Oka K, Iwata S, Ohnishi T, (2007) Silencing hypoxia-inducible factor-1alpha inhibits cell migration and invasion under hypoxic environment in malignant gliomas. Int J Oncol 30: 793-802
16. Hanahan D, Folkman J, (1996) Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell 86: 353-364
17. Harada H, Kizaka-Kondoh S, Itasaka S, Shibuya K, Morinibu A, Shinomiya K, Hiraoka M, (2007) The combination of hypoxia-response enhancers and an oxygen-dependent proteolytic motif enables real-time imaging of absolute HIF-1 activity in tumor xenografts. Biochem Biophys Res Commun 360: 791-796
18. Heim R, Prasher DC, Tsien RY, (1994) Wavelength mutations and posttranslational autoxidation of green fluorescent protein. Proc Natl Acad Sci USA 91: 12501-12504
19. Hendriksen EM, Span PN, Schuuring J, Peters JP, Sweep FC, van der Kogel AJ, Bussink J, (2009) Angiogenesis, hypoxia and VEGF expression during tumour growth in a human xenograft tumour model. Microvasc Res 77: 96-103
20. Hockel M, Vaupel P, (2001) Tumor hypoxia: definitions and current clinical, biologic, and molecular aspects. J Natl Cancer Inst 93: 266-276
21. Holtmaat A, Bonhoeffer T, Chow DK, Chuckowree J, De Paola V, Hofer SB, Hubener M, Keck T, Knott G, Lee WC, Mostany R, Mrsic-Flogel TD, Nedivi E, Portera-Cailliau C, Svoboda K, Trachtenberg JT, Wilbrecht L, (2009) Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window. Nat Protoc 4: 1128-1144
22. Janssen HL, Haustermans KM, Sprong D, Blommestijn G, Hofland I, Hoebers FJ, Blijweert E, Raleigh JA, Semenza GL, Varia MA, Balm AJ, van Velthuysen ML, Delaere P, Sciot R, Begg AC, (2002) HIF-1A, pimonidazole, and iododeoxyuridine to estimate hypoxia and perfusion in human head-and-neck tumors. Int J Radiat Oncol Biol Phys 54: 1537-1549
23. Kiyose K, Hanaoka K, Oushiki D, Nakamura T, Kajimura M, Suematsu M, Nishimatsu H, Yamane T, Terai T, Hirata Y, Nagano T, (2010) Hypoxia-sensitive fluorescent probes for in vivo real-time fluorescence imaging of acute ischemia. J Am Chem Soc 132: 15846-15848
24. Kizaka-Kondoh S, Konse-Nagasawa H, (2009) Significance of nitroimidazole compounds and hypoxia-inducible factor-1 for imaging tumor hypoxia. Cancer Sci 100: 1366-1373
25. Kumagai A, Ando R, Miyatake H, Greimel P, Kobayashi T, Hirabayashi Y, Shimogori T, Miyawaki A, (2013) A bilirubin-inducible fluorescent protein from eel muscle. Cell 153: 1602-1611
26. Lando D, Peet DJ, Gorman JJ, Whelan DA, Whitelaw ML, Bruick RK, (2002) FIH-1 is an asparaginyl hydroxylase enzyme that regulates the transcriptional activity of hypoxia-inducible factor. Genes Dev 16: 1466-1471
27. Lecoq J, Parpaleix A, Roussakis E, Ducros M, Goulam HY, Vinogradov SA, Charpak S, (2011) Simultaneous two-photon imaging of oxygen and blood flow in deep cerebral vessels. Nat Med 17: 893-898
28. Li X, Zhao X, Fang Y, Jiang X, Duong T, Fan C, Huang CC, Kain SR, (1998) Generation of destabilized green fluorescent protein as a transcription reporter. J Biol Chem 273: 34970-34975
29. Malhotra R, Lin Z, Vincenz C, Brosius FC III, (2001) Hypoxia induces apoptosis via two independent pathways in Jurkat cells: differential regulation by glucose. Am J Physiol Cell Physiol 281: C1596-C1603
30. Mathieu J, Zhang Z, Nelson A, Lamba DA, Reh TA, Ware C, Ruohola-Baker H, (2013) Hypoxia induces re-entry of committed cells into pluripotency. Stem Cells 31: 1737-1748
31. Mishin AS, Belousov VV, Solntsev KM, Lukyanov KA, (2015) Novel uses of fluorescent proteins. Curr Opin Chem Biol 27: 1-9
32. Muz B, de la Puente P, Azab F, Luderer M, Azab AK, (2014) Hypoxia promotes stem cell-like phenotype in multiple myeloma cells. Blood Cancer J 4: e262
33. Raleigh JA, Dewhirst MW, Thrall DE, (1996) Measuring tumor hypoxia. Semin Radiat Oncol 6: 37-45
34. Remington SJ, (2006) Fluorescent proteins: maturation, photochemistry and photophysics. Curr Opin Struct Biol 16: 714-721
35. Revuelta-Lopez E, Castellano J, Roura S, Galvez-Monton C, Nasarre L, Benitez S, Bayes-Genis A, Badimon L, Llorente-Cortes V, (2013) Hypoxia induces metalloproteinase-9 activation and human vascular smooth muscle cell migration through low-density lipoprotein receptor-related protein 1-mediated Pyk2 phosphorylation. Arterioscler Thromb Vasc Biol 33: 2877-2887
36. Rogers S, Wells R, Rechsteiner M, (1986) Amino acid sequences common to rapidly degraded proteins: the PEST hypothesis. Science 234: 364-368
37. Roussakis E, Spencer JA, Lin CP, Vinogradov SA, (2014) Two-photon antenna-core oxygen probe with enhanced performance. Anal Chem 86: 5937-5945
38. Salceda S, Caro J, (1997) Hypoxia-inducible factor 1alpha (HIF-1alpha) protein is rapidly degraded by the ubiquitin-proteasome system under normoxic conditions. Its stabilization by hypoxia depends on redox-induced changes. J Biol Chem 272: 22642-22647
39. Semenza GL, (2011) Oxygen sensing, homeostasis, and disease. N Engl J Med 365: 537-547
40. Semenza GL, (2012) Hypoxia-inducible factors: mediators of cancer progression and targets for cancer therapy. Trends Pharmacol Sci 33: 207-214
41. Semenza GL, Nejfelt MK, Chi SM, Antonarakis SE, (1991) Hypoxia-inducible nuclear factors bind to an enhancer element located 3′ to the human erythropoietin gene. Proc Natl Acad Sci USA 88: 5680-5684
42. Shaner NC, Steinbach PA, Tsien RY, (2005) A guide to choosing fluorescent proteins. Nat Methods 2: 905-909
43. Shibata T, Giaccia AJ, Brown JM, (2000) Development of a hypoxia-responsive vector for tumor-specific gene therapy. Gene Ther 7: 493-498
44. Span PN, Bussink J, (2015) Biology of hypoxia. Semin Nucl Med 45: 101-109
45. Spencer JA, Ferraro F, Roussakis E, Klein A, Wu J, Runnels JM, Zaher W, Mortensen LJ, Alt C, Turcotte R, Yusuf R, Cote D, Vinogradov SA, Scadden DT, Lin CP, (2014) Direct measurement of local oxygen concentration in the bone marrow of live animals. Nature 508: 269-273
46. Srinivas V, Zhang LP, Zhu XH, Caro J, (1999) Characterization of an oxygen/redox-dependent degradation domain of hypoxia-inducible factor alpha (HIF-alpha) proteins. Biochem Biophys Res Commun 260: 557-561
47. Vordermark D, Shibata T, Brown JM, (2001) Green fluorescent protein is a suitable reporter of tumor hypoxia despite an oxygen requirement for chromophore formation. Neoplasia 3: 527-534
48. Wenger RH, Stiehl DP, Camenisch G, (2005) Integration of oxygen signaling at the consensus HRE. Sci STKE 2005: re12
49. Yuan Y, Hilliard G, Ferguson T, Millhorn DE, (2003) Cobalt inhibits the interaction between hypoxia-inducible factor-alpha and von Hippel-Lindau protein by direct binding to hypoxia-inducible factor-alpha. J Biol Chem 278: 15911-15916