Cytometry-based single-cell analysis of intact epithelial signaling reveals MAPK activation divergent from TNF-α-induced apoptosis in vivo

Molecular Systems Biology

Volumn 11, Issue 10, 2015, Pages

  Simmons, Alan J ^a,b   Banerjee, Amrita ^a,b   McKinley, Eliot T ^a   Scurrah, Cherie R ^a,b   Herring, Charles A ^a,b   Gewin, Leslie S ^a,b,c   Masuzaki, Ryota ^a   Karp, Seth J ^a   Franklin, Jeffrey L ^a,b   Gerdes, Michael J ^d   Irish, Jonathan M ^a   Coffey, Robert J ^a,b,c   Lau, Ken S ^a,b  

^a VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

^d GE GLOBAL RESEARCH   (United States)

Author keywords

apoptosis; CyTOF; epithelial signaling; single cell biology; TNF

Indexed keywords

CELL MARKER; MITOGEN ACTIVATED PROTEIN KINASE; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL POPULATION; CELL SURVIVAL; CONTROLLED STUDY; CYTOMETRY; CYTOMETRY TIME OF FLIGHT; ENZYME ACTIVATION; EPITHELIUM CELL; FEMALE; FLOW CYTOMETRY; FLUORESCENCE; IN VIVO STUDY; INTESTINE CELL; INTESTINE EPITHELIUM; INTRACELLULAR SIGNALING; MOUSE; NONHUMAN; PRIORITY JOURNAL; SINGLE CELL ANALYSIS; HUMAN; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION;

APOPTOSIS; ENZYME ACTIVATION; EPITHELIAL CELLS; HUMANS; MAP KINASE SIGNALING SYSTEM; SIGNAL TRANSDUCTION; SINGLE-CELL ANALYSIS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84945973720     PISSN: None     EISSN: 17444292     Source Type: Journal    
DOI: 10.15252/msb.20156282     Document Type: Article

References (59)

1. Abrahamsen I, Lorens JB, (2013) Evaluating extracellular matrix influence on adherent cell signaling by cold trypsin phosphorylation-specific flow cytometry. BMC Cell Biol 14: 36
2. Amir E-AD, Davis KL, Tadmor MD, Simonds EF, Levine JH, Bendall SC, Shenfeld DK, Krishnaswamy S, Nolan GP, Pe'er D, (2013) viSNE enables visualization of high dimensional single-cell data and reveals phenotypic heterogeneity of leukemia. Nat Biotechnol 31: 545-552
3. Angelo M, Bendall SC, Finck R, Hale MB, Hitzman C, Borowsky AD, Levenson RM, Lowe JB, Liu SD, Zhao S, Natkunam Y, Nolan GP, (2014) Multiplexed ion beam imaging of human breast tumors. Nat Med 20: 436-442
4. Bates MD, Erwin CR, Sanford LP, Wiginton D, Bezerra JA, Schatzman LC, Jegga AG, Ley-Ebert C, Williams SS, Steinbrecher KA, Warner BW, Cohen MB, Aronow BJ, (2002) Novel genes and functional relationships in the adult mouse gastrointestinal tract identified by microarray analysis. Gastroenterology 122: 1467-1482
5. Baum B, Georgiou M, (2011) Dynamics of adherens junctions in epithelial establishment, maintenance, and remodeling. J Cell Biol 192: 907-917
6. Bendall SC, Simonds EF, Qiu P, Amir ED, Krutzik PO, Finck R, Bruggner RV, Melamed R, Trejo A, Ornatsky OI, Balderas RS, Plevritis SK, Sachs K, Pe'er D, Tanner SD, Nolan GP, (2011) Single-cell mass cytometry of differential immune and drug responses across a human hematopoietic continuum. Science 332: 687-696
7. Bendall SC, Davis KL, Amir EAD, Tadmor MD, Simonds EF, Chen TJ, Shenfeld DK, Nolan GP, Pe'er D, (2014) Single-cell trajectory detection uncovers progression and regulatory coordination in human b cell development. Cell 157: 714-725
8. Bian ZM, Elner SG, Yoshida a, Kunkel SL, Su J, Elner VM, (2001) Activation of p38, ERK1/2 and NIK pathways is required for IL-1beta and TNF-alpha-induced chemokine expression in human retinal pigment epithelial cells. Exp Eye Res 73: 111-121
9. Boyd-Tressler A, Penuela S, Laird DW, Dubyak GR, (2014) Chemotherapeutic drugs induce ATP release via caspase-gated pannexin-1 channels and a caspase/pannexin-1-independent mechanism. J Biol Chem 289: 27246-27263
10. Chaudhary R, Ghosh S, (2005) Infliximab in refractory coeliac disease. Eur J Gastroenterol Hepatol 17: 603-604
11. Cheng H, Leblond CP, (1974) Origin, differentiation and renewal of the four main epithelial cell types in the mouse small intestine. I. Columnar cell. Am J Anat 141: 461-479
12. Colombel JF, Sandborn WJ, Reinisch W, Mantzaris GJ, Kornbluth A, Rachmilewitz D, Lichtiger S, D'Haens G, Diamond RH, Broussard DL, Tang KL, van der Woude CJ, Rutgeerts P, (2010) Infliximab, azathioprine, or combination therapy for Crohn's disease. N Engl J Med 362: 1383-1395
13. Fatehullah A, Appleton PL, Näthke IS, (2013) Cell and tissue polarity in the intestinal tract during tumourigenesis: cells still know the right way up, but tissue organization is lost. Philos Trans R Soc Lond B Biol Sci 368: 20130014
14. Gage GJ, Kipke DR, Shain W, (2012) Whole animal perfusion fixation for rodents. J Vis Exp 65: e3564
15. Gerbe F, van Es JH, Makrini L, Brulin B, Mellitzer G, Robine S, Romagnolo B, Shroyer NF, Bourgaux J-F, Pignodel C, Clevers H, Jay P, (2011) Distinct ATOH1 and Neurog3 requirements define tuft cells as a new secretory cell type in the intestinal epithelium. J Cell Biol 192: 767-780
16. Gerbe F, Legraverend C, Jay P, (2012) The intestinal epithelium tuft cells: specification and function. Cell Mol Life Sci 69: 2907-2917
17. Gerdes MJ, Sevinsky CJ, Sood A, Adak S, Bello MO, Bordwell A, Can A, Corwin A, Dinn S, Filkins RJ, Hollman D, Kamath V, Kaanumalle S, Kenny K, Larsen M, Lazare M, Li Q, Lowes C, McCulloch CC, McDonough E, et al, (2013) Highly multiplexed single-cell analysis of formalin-fixed, paraffin-embedded cancer tissue. Proc Natl Acad Sci USA 110: 11982-11987
18. Gewin L, Bulus N, Mernaugh G, Moeckel G, Harris RC, Moses HL, Pozzi A, Zent R, (2010) TGF-beta receptor deletion in the renal collecting system exacerbates fibrosis. J Am Soc Nephrol 21: 1334-1343
19. Giacinti C, Giordano A, (2006) RB and cell cycle progression. Oncogene 25: 5220-5227
20. Giesen C, Wang H, Schapiro D, Zivanovic N, Jacobs A, Hattendorf B, Schüffler PJ, Grolimund D, Buhmann JM, Brandt S, Varga Z, Wild PJ, Günther D, Bodenmiller B, (2014) Highly multiplexed imaging of tumor tissues with subcellular resolution by mass cytometry. Nat Methods 11: 417-422
21. Gunawardene AR, Corfe BM, Staton CA, (2011) Classification and functions of enteroendocrine cells of the lower gastrointestinal tract. Int J Exp Pathol 92: 219-231
22. Halpern MD, Clark J, Saunders T, Doelle SM, Hosseini DM, Stagner AM, Dvorak B, (2006) Reduction of experimental necrotizing enterocolitis with anti-TNF-alpha. Am J Physiol Gastrointest Liver Physiol 290: G757-G764
23. Ho AWY, Wong CK, Lam CWK, (2008) Tumor necrosis factor-alpha up-regulates the expression of CCL2 and adhesion molecules of human proximal tubular epithelial cells through MAPK signaling pathways. Immunobiology 213: 533-544
24. Imajo M, Ebisuya M, Nishida E, (2014) Dual role of YAP and TAZ in renewal of the intestinal epithelium. Nat Cell Biol 17: 7-19
25. Irish JM, Hovland R, Krutzik PO, Perez OD, Bruserud Ø, Gjertsen BT, Nolan GP, (2004) Single cell profiling of potentiated phospho-protein networks in cancer cells. Cell 118: 217-228
26. Itzkovitz S, Lyubimova A, Blat IC, Maynard M, van Es J, Lees J, Jacks T, Clevers H, van Oudenaarden A, (2011) Single-molecule transcript counting of stem-cell markers in the mouse intestine. Nat Cell Biol 14: 106-114
27. Jijon HB, Walker J, Hoentjen F, Diaz H, Ewaschuk J, Jobin C, Madsen KL, (2005) Adenosine is a negative regulator of NF-κB and MAPK signaling in human intestinal epithelial cells. Cell Immunol 237: 86-95
28. Kawamura S, Miyamoto S, Brown JH, (2003) Initiation and transduction of stretch-induced RhoA and Rac1 activation through caveolae. Cytoskeletal regulation of ERK translocation. J Biol Chem 278: 31111-31117
29. Kim J-A, Kim D-K, Kang O-H, Choi Y-A, Park H-J, Choi S-C, Kim T-H, Yun K-J, Nah Y-H, Lee Y-M, (2005) Inhibitory effect of luteolin on TNF-alpha-induced IL-8 production in human colon epithelial cells. Int Immunopharmacol 5: 209-217
30. Krutzik PO, Irish JM, Nolan GP, Perez OD, (2004) Analysis of protein phosphorylation and cellular signaling events by flow cytometry: techniques and clinical applications. Clin Immunol 110: 206-221
31. Lau KS, Partridge EA, Grigorian A, Silvescu CI, Reinhold VN, Demetriou M, Dennis JW, (2007) Complex N-glycan number and degree of branching cooperate to regulate cell proliferation and differentiation. Cell 129: 123-134
32. Lau KS, Juchheim AM, Cavaliere KR, Philips SR, Lauffenburger DA, Haigis KM, (2011) In vivo systems analysis identifies spatial and temporal aspects of the modulation of TNF-α-induced apoptosis and proliferation by MAPKs. Sci Signal 4: ra16
33. Lau KS, Cortez-Retamozo V, Philips SR, Pittet MJ, Lauffenburger DA, Haigis KM, (2012) Multi-scale in vivo systems analysis reveals the influence of immune cells on TNF-α-induced apoptosis in the intestinal epithelium. PLoS Biol 10: e1001393
34. Lau KS, Schrier SB, Gierut J, Lyons J, Lauffenburger DA, Haigis KM, (2013) Network analysis of differential Ras isoform mutation effects on intestinal epithelial responses to TNF-α. Integr Biol 5: 1355-1365
35. Li F, Huang Q, Chen J, Peng Y, Roop DR, Bedford JS, Li C-Y, (2010) Apoptotic cells activate the "phoenix rising" pathway to promote wound healing and tissue regeneration. Sci Signal 3: ra13
36. Lin CC, Huang WL, Su WP, Chen HHW, Lai WW, Yan JJ, Su WC, (2010) Single cell phospho-specific flow cytometry can detect dynamic changes of phospho-Stat1 level in lung cancer cells. Cytom Part A 77: 1008-1019
37. Magness ST, Puthoff BJ, Crissey MA, Dunn J, Henning SJ, Houchen C, Kaddis JS, Kuo CJ, Li L, Lynch J, Martin MG, May R, Niland JC, Olack B, Qian D, Stelzner M, Swain JR, Wang F, Wang J, Wang X, et al, (2013) A multicenter study to standardize reporting and analyses of fluorescence-activated cell-sorted murine intestinal epithelial cells. Am J Physiol Gastrointest Liver Physiol 305: G542-G551
38. Monier B, Gettings M, Gay G, Mangeat T, Schott S, Guarner A, Suzanne M, (2015) Apico-basal forces exerted by apoptotic cells drive epithelium folding. Nature 518: 245-248
39. O'Donnell EA, Ernst DN, Hingorani R, (2013) Multiparameter flow cytometry: advances in high resolution analysis. Immune Netw 13: 43-54
40. Patel VA, Massenburg D, Vujicic S, Feng L, Tang M, Litbarg N, Antoni A, Rauch J, Lieberthal W, Levine JS, (2015) Apoptotic cells activate AMPK and inhibit epithelial cell growth without change in intracellular energy stores. J Biol Chem 290: 22352-22369
41. Paulus U, Loeffler M, Zeidler J, Owen G, Potten CS, (1993) The differentiation and lineage development of goblet cells in the murine small intestinal crypt: experimental and modelling studies. J Cell Sci 106: 473-483
42. Pieters T, van Roy F, van Hengel J, (2012) Functions of p120ctn isoforms in cell-cell adhesion and intracellular signaling. Front Biosci 17: 1669-1694
43. Poulin EJ, Powell AE, Wang Y, Li Y, Franklin JL, Coffey RJ, (2014) Using a new Lrig1 reporter mouse to assess differences between two Lrig1 antibodies in the intestine. Stem Cell Res 13: 422-430
44. Powell AE, Wang Y, Li Y, Poulin EJ, Means AL, Washington MK, Higginbotham JN, Juchheim A, Prasad N, Levy SE, Guo Y, Shyr Y, Aronow BJ, Haigis KM, Franklin JL, Coffey RJ, (2012) The pan-ErbB negative regulator Lrig1 is an intestinal stem cell marker that functions as a tumor suppressor. Cell 149: 146-158
45. Qi Z, Shen L, Zhou H, Jiang Y, Lan L, Luo L, Yin Z, (2014) Phosphorylation of heat shock protein 27 antagonizes TNF-alpha induced HeLa cell apoptosis via regulating TAK1 ubiquitination and activation of p38 and ERK signaling. Cell Signal 26: 1616-1625
46. Rojanapo W, Lamb AJ, Olson JA, (1980) The prevalence, metabolism and migration of goblet cells in rat intestine following the induction of rapid, synchronous vitamin A deficiency. J Nutr 110: 178-188
47. Rosenblatt J, Raff MC, Cramer LP, (2001) An epithelial cell destined for apoptosis signals its neighbors to extrude it by an actin- and myosin-dependent mechanism. Curr Biol 11: 1847-1857
48. Saez-Rodriguez J, Alexopoulos LG, Epperlein J, Samaga R, Lauffenburger DA, Klamt S, Sorger PK, (2009) Discrete logic modelling as a means to link protein signalling networks with functional analysis of mammalian signal transduction. Mol Syst Biol 5: 331
49. Sato T, van Es JH, Snippert HJ, Stange DE, Vries RG, van den Born M, Barker N, Shroyer NF, van de Wetering M, Clevers H, (2011) Paneth cells constitute the niche for Lgr5 stem cells in intestinal crypts. Nature 469: 415-418
50. Schütze S, Tchikov V, Schneider-Brachert W, (2008) Regulation of TNFR1 and CD95 signalling by receptor compartmentalization. Nat Rev Mol Cell Biol 9: 655-662
51. Song KS, Lee WJ, Chung KC, Koo JS, Yang EJ, Choi JY, Yoon JH, (2003) Interleukin-1beta and tumor necrosis factor-alpha induce MUC5AC overexpression through a mechanism involving ERK/p38 mitogen-activated protein kinases-MSK1-CREB activation in human airway epithelial cells. J Biol Chem 278: 23243-23250
52. Trapnell C, Cacchiarelli D, Grimsby J, Pokharel P, Li S, Morse M, Lennon NJ, Livak KJ, Mikkelsen TS, Rinn JL, (2014) The dynamics and regulators of cell fate decisions are revealed by pseudotemporal ordering of single cells. Nat Biotechnol 32: 381-386
53. Van der Flier LG, Clevers H, (2009) Stem cells, self-renewal, and differentiation in the intestinal epithelium. Annu Rev Physiol 71: 241-260
54. Williams JM, Duckworth CA, Watson AJM, Frey MR, Miguel JC, Burkitt MD, Sutton R, Hughes KR, Hall LJ, Caamaño JH, Campbell BJ, Pritchard DM, (2013) A mouse model of pathological small intestinal epithelial cell apoptosis and shedding induced by systemic administration of lipopolysaccharide. Dis Model Mech 6: 1388-1399
55. Wright N, Alison M, (1984) The biology of epithelial cell populations. Oxford: Clarendon Press
56. Wu H, Wang G, Li S, Zhang M, Li H, Wang K, (2015) TNF-a- mediated-p38-dependent signaling pathway contributes to myocyte apoptosis in rats subjected to surgical trauma. Cell Physiol Biochem 150081: 1454-1466
57. Xing Y, Su TT, Ruohola-baker H, (2015) Tie-mediated signal from apoptotic cells protects stem cells in Drosophila melanogaster. Nat Commun 6: 7058
58. Yamashita S, (2007) Heat-induced antigen retrieval: mechanisms and application to histochemistry. Prog Histochem Cytochem 41: 141-200
59. Yu L, Zhao Y, Xu S, Jin C, Wang M, Fu G, (2014) Leptin confers protection against TNF-α-induced apoptosis in rat cardiomyocytes. Biochem Biophys Res Commun 455: 126-132