Macrophage-associated wound healing contributes to African green monkey SIV pathogenesis control

Fredrik Barrenas; Kevin Raehtz; Cuiling Xu; Lynn Law; Richard R. Green; Guido Silvestri; Steven E. Bosinger; Andrew Nishida; Qingsheng Li; Wuxun Lu; Jianshui Zhang; Matthew J. Thomas; Jean Chang; Elise Smith; Jeffrey M. Weiss; Reem A. Dawoud; George H. Richter; Anita Trichel; Dongzhu Ma; Xinxia Peng; Jan Komorowski; Cristian Apetrei; Ivona Pandrea; Michael Gale

doi:10.1038/s41467-019-12987-9

Macrophage-associated wound healing contributes to African green monkey SIV pathogenesis control

Fredrik Barrenas, Kevin Raehtz, Cuiling Xu, Lynn Law, Richard R. Green, Guido Silvestri, Steven E. Bosinger, Andrew Nishida, Qingsheng Li, Wuxun Lu, Jianshui Zhang, Matthew J. Thomas, Jean Chang, Elise Smith, Jeffrey M. Weiss, Reem A. Dawoud, George H. Richter, Anita Trichel, Dongzhu Ma, Xinxia PengJan Komorowski, Cristian Apetrei, Ivona Pandrea, Michael Gale

Research output: Contribution to journal › Article › peer-review

1 Scopus citations

Abstract

Natural hosts of simian immunodeficiency virus (SIV) avoid AIDS despite lifelong infection. Here, we examined how this outcome is achieved by comparing a natural SIV host, African green monkey (AGM) to an AIDS susceptible species, rhesus macaque (RM). To asses gene expression profiles from acutely SIV infected AGMs and RMs, we developed a systems biology approach termed Conserved Gene Signature Analysis (CGSA), which compared RNA sequencing data from rectal AGM and RM tissues to various other species. We found that AGMs rapidly activate, and then maintain, evolutionarily conserved regenerative wound healing mechanisms in mucosal tissue. The wound healing protein fibronectin shows distinct tissue distribution and abundance kinetics in AGMs. Furthermore, AGM monocytes exhibit an embryonic development and repair/regeneration signature featuring TGF-β and concomitant reduced expression of inflammatory genes compared to RMs. This regenerative wound healing process likely preserves mucosal integrity and prevents inflammatory insults that underlie immune exhaustion in RMs.

Original language	English (US)
Article number	5101
Journal	Nature communications
Volume	10
Issue number	1
DOIs	https://doi.org/10.1038/s41467-019-12987-9
State	Published - Dec 1 2019

ASJC Scopus subject areas

Chemistry(all)
Biochemistry, Genetics and Molecular Biology(all)
Physics and Astronomy(all)

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Barrenas, F., Raehtz, K., Xu, C., Law, L., Green, R. R., Silvestri, G., Bosinger, S. E., Nishida, A., Li, Q., Lu, W., Zhang, J., Thomas, M. J., Chang, J., Smith, E., Weiss, J. M., Dawoud, R. A., Richter, G. H., Trichel, A., Ma, D., ... Gale, M. (2019). Macrophage-associated wound healing contributes to African green monkey SIV pathogenesis control. Nature communications, 10(1), [5101]. https://doi.org/10.1038/s41467-019-12987-9

Macrophage-associated wound healing contributes to African green monkey SIV pathogenesis control. / Barrenas, Fredrik; Raehtz, Kevin; Xu, Cuiling; Law, Lynn; Green, Richard R.; Silvestri, Guido; Bosinger, Steven E.; Nishida, Andrew; Li, Qingsheng; Lu, Wuxun; Zhang, Jianshui; Thomas, Matthew J.; Chang, Jean; Smith, Elise; Weiss, Jeffrey M.; Dawoud, Reem A.; Richter, George H.; Trichel, Anita; Ma, Dongzhu; Peng, Xinxia; Komorowski, Jan; Apetrei, Cristian; Pandrea, Ivona; Gale, Michael.

In: Nature communications, Vol. 10, No. 1, 5101, 01.12.2019.

Research output: Contribution to journal › Article › peer-review

Barrenas, F, Raehtz, K, Xu, C, Law, L, Green, RR, Silvestri, G, Bosinger, SE, Nishida, A, Li, Q, Lu, W, Zhang, J, Thomas, MJ, Chang, J, Smith, E, Weiss, JM, Dawoud, RA, Richter, GH, Trichel, A, Ma, D, Peng, X, Komorowski, J, Apetrei, C, Pandrea, I & Gale, M 2019, 'Macrophage-associated wound healing contributes to African green monkey SIV pathogenesis control', Nature communications, vol. 10, no. 1, 5101. https://doi.org/10.1038/s41467-019-12987-9

Barrenas, Fredrik ; Raehtz, Kevin ; Xu, Cuiling ; Law, Lynn ; Green, Richard R. ; Silvestri, Guido ; Bosinger, Steven E. ; Nishida, Andrew ; Li, Qingsheng ; Lu, Wuxun ; Zhang, Jianshui ; Thomas, Matthew J. ; Chang, Jean ; Smith, Elise ; Weiss, Jeffrey M. ; Dawoud, Reem A. ; Richter, George H. ; Trichel, Anita ; Ma, Dongzhu ; Peng, Xinxia ; Komorowski, Jan ; Apetrei, Cristian ; Pandrea, Ivona ; Gale, Michael. / Macrophage-associated wound healing contributes to African green monkey SIV pathogenesis control. In: Nature communications. 2019 ; Vol. 10, No. 1.

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title = "Macrophage-associated wound healing contributes to African green monkey SIV pathogenesis control",

abstract = "Natural hosts of simian immunodeficiency virus (SIV) avoid AIDS despite lifelong infection. Here, we examined how this outcome is achieved by comparing a natural SIV host, African green monkey (AGM) to an AIDS susceptible species, rhesus macaque (RM). To asses gene expression profiles from acutely SIV infected AGMs and RMs, we developed a systems biology approach termed Conserved Gene Signature Analysis (CGSA), which compared RNA sequencing data from rectal AGM and RM tissues to various other species. We found that AGMs rapidly activate, and then maintain, evolutionarily conserved regenerative wound healing mechanisms in mucosal tissue. The wound healing protein fibronectin shows distinct tissue distribution and abundance kinetics in AGMs. Furthermore, AGM monocytes exhibit an embryonic development and repair/regeneration signature featuring TGF-β and concomitant reduced expression of inflammatory genes compared to RMs. This regenerative wound healing process likely preserves mucosal integrity and prevents inflammatory insults that underlie immune exhaustion in RMs.",

author = "Fredrik Barrenas and Kevin Raehtz and Cuiling Xu and Lynn Law and Green, {Richard R.} and Guido Silvestri and Bosinger, {Steven E.} and Andrew Nishida and Qingsheng Li and Wuxun Lu and Jianshui Zhang and Thomas, {Matthew J.} and Jean Chang and Elise Smith and Weiss, {Jeffrey M.} and Dawoud, {Reem A.} and Richter, {George H.} and Anita Trichel and Dongzhu Ma and Xinxia Peng and Jan Komorowski and Cristian Apetrei and Ivona Pandrea and Michael Gale",

note = "Funding Information: We would like to thank Michael Katze and Robert Palermo for their input during the early stages of this study. This work was supported by the National Institutes of Health, Office of the Director P51OD010425, R24OD011157, and R24OD011172; University of Washington Center for Innate Immunity and Immune Disease; NIAID contract no. HHSN272201300010C; an NIAID Simian Vaccine Evaluation Unit contract with the University of Washington (contract no. N01-AI-60006); NIDDK, NCRR and NHLBI, NIH (R01 DK087625-01. to Q.L., R24-OD010445 to S.E.B. and G.S., RR025781, DK108837, R01HL117715, R01HL123096, R01DK113919, R01AI119346 to I.P. and C.A.); the Preclinical Research & Development Branch, VRP, DAIDS, NIAID, NIH (task order under N01-AI-30018 to Q.L.); the DAIDS Reagent Resource Support Program for AIDS Vaccine Development, Quality Biological, Gaithersburg, MD, Division of AIDS (contract no. N01-A30018); National Institutes of Health Training Grant T32 AI065380-08 and AI065380-09 (to K.R.) and the Swedish Research Council (D0045701) and eSSENCE (to F.B.).",

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doi = "10.1038/s41467-019-12987-9",

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AU - Barrenas, Fredrik

AU - Raehtz, Kevin

AU - Xu, Cuiling

AU - Law, Lynn

AU - Green, Richard R.

AU - Silvestri, Guido

AU - Bosinger, Steven E.

AU - Nishida, Andrew

AU - Li, Qingsheng

AU - Lu, Wuxun

AU - Zhang, Jianshui

AU - Thomas, Matthew J.

AU - Chang, Jean

AU - Smith, Elise

AU - Weiss, Jeffrey M.

AU - Dawoud, Reem A.

AU - Richter, George H.

AU - Trichel, Anita

AU - Ma, Dongzhu

AU - Peng, Xinxia

AU - Komorowski, Jan

AU - Apetrei, Cristian

AU - Pandrea, Ivona

AU - Gale, Michael

N1 - Funding Information: We would like to thank Michael Katze and Robert Palermo for their input during the early stages of this study. This work was supported by the National Institutes of Health, Office of the Director P51OD010425, R24OD011157, and R24OD011172; University of Washington Center for Innate Immunity and Immune Disease; NIAID contract no. HHSN272201300010C; an NIAID Simian Vaccine Evaluation Unit contract with the University of Washington (contract no. N01-AI-60006); NIDDK, NCRR and NHLBI, NIH (R01 DK087625-01. to Q.L., R24-OD010445 to S.E.B. and G.S., RR025781, DK108837, R01HL117715, R01HL123096, R01DK113919, R01AI119346 to I.P. and C.A.); the Preclinical Research & Development Branch, VRP, DAIDS, NIAID, NIH (task order under N01-AI-30018 to Q.L.); the DAIDS Reagent Resource Support Program for AIDS Vaccine Development, Quality Biological, Gaithersburg, MD, Division of AIDS (contract no. N01-A30018); National Institutes of Health Training Grant T32 AI065380-08 and AI065380-09 (to K.R.) and the Swedish Research Council (D0045701) and eSSENCE (to F.B.).

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N2 - Natural hosts of simian immunodeficiency virus (SIV) avoid AIDS despite lifelong infection. Here, we examined how this outcome is achieved by comparing a natural SIV host, African green monkey (AGM) to an AIDS susceptible species, rhesus macaque (RM). To asses gene expression profiles from acutely SIV infected AGMs and RMs, we developed a systems biology approach termed Conserved Gene Signature Analysis (CGSA), which compared RNA sequencing data from rectal AGM and RM tissues to various other species. We found that AGMs rapidly activate, and then maintain, evolutionarily conserved regenerative wound healing mechanisms in mucosal tissue. The wound healing protein fibronectin shows distinct tissue distribution and abundance kinetics in AGMs. Furthermore, AGM monocytes exhibit an embryonic development and repair/regeneration signature featuring TGF-β and concomitant reduced expression of inflammatory genes compared to RMs. This regenerative wound healing process likely preserves mucosal integrity and prevents inflammatory insults that underlie immune exhaustion in RMs.

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