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Evidence for cross-talk between atrial natriuretic peptide and nitric oxide receptors

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Abstract

Guanylyl cyclases (GCs), a ubiquitous family of enzymes that metabolize GTP to cyclic GMP (cGMP), are traditionally divided into membrane-bound forms (GC-A-G) that are activated by peptides and cytosolic forms that are activated by nitric oxide (NO) and carbon monoxide. However, recent data has shown that NO activated GC’s (NOGC) also may be associated with membranes. In the present study, interactions of guanylyl cyclase A (GC-A), a caveolae-associated, membrane-bound, homodimer activated by atrial natriuretic peptide (ANP), with NOGC, a heme-containing heterodimer (α/β) β1 isoform of the β subunit of NOGC (NOGCβ1) was specifically focused. NOGCβ1 co-localized with GC-A and caveolin on the membrane in human kidney (HK-2) cells. Interaction of GC-A with NOGCβ1 was found using immunoprecipitations. In a second set of experiments, the possibility that NOGCβ1 regulates signaling by GC-A in HK-2 cells was explored. ANP-stimulated membrane guanylyl cyclase activity (0.05 ± 0.006 pmol/mg protein/5 min; P < 0.01) and intra cellular GMP (18.1 ± 3.4 vs. 1.2 ± 0.5 pmol/mg protein; P < 0.01) were reduced in cells in which NOGCβ1 abundance was reduced using specific siRNA to NOGCβ1. On the other hand, ANP-stimulated cGMP formation was increased in cells transiently transfected with NOGCβ1 (530.2 ± 141.4 vs. 26.1 ± 13.6 pmol/mg protein; P < 0.01). siRNA to NOGCβ1 attenuated inhibition of basolateral Na/K ATPase activity by ANP (192 ± 22 vs. 92 ± 9 nmol phosphate/mg protein/min; P < 0.05). In summary, the results show that NOGCβ1 and GC-A interact and that NOGCβ1 regulates ANP signaling in HK-2 cells. The results raise the novel possibility of cross-talk between NOGC and GC-A signaling pathways in membrane caveolae.

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Acknowledgments

Support: National Institute of Health H R21DK065628-02 (to RSD); American Heart Association Grant-in-Aid (to RSD); Tobacco Research Institute (to RSD); National Institute of Health K01 DK071641-03 (to KUK).

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Authors and Affiliations

  1. Department of Medicine, University of Illinois at Chicago, Jesse Brown VA Medical Center, 820 S. Damen Avenue, Chicago, IL, 60612, USA

    Kumar U. Kotlo & Robert S. Danziger

  2. Department of Physiology and Biophysics, University of Illinois at Chicago, 2095 COMRB, Chicago, IL, 60612, USA

    Mark M. Rasenick

  3. Department of Psychiatry, University of Illinois at Chicago, 2095 COMRB, Chicago, IL, 60612, USA

    Mark M. Rasenick

  4. Department of Physiology and Biophysics, University of Illinois at Chicago, Jesse Brown VA Medical Center, 820 S. Damen Avenue, Chicago, IL, 60612, USA

    Robert S. Danziger

  5. Department of Pharmacology, University of Illinois at Chicago, Jesse Brown VA Medical Center, 820 S. Damen Avenue, Chicago, IL, 60612, USA

    Robert S. Danziger

  6. Division of Cardiology, University of Illinois at Chicago, 840 S. Wood St., MC 715, Chicago, IL, 60612, USA

    Kumar U. Kotlo

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  1. Kumar U. Kotlo
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Correspondence to Kumar U. Kotlo.

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Kotlo, K.U., Rasenick, M.M. & Danziger, R.S. Evidence for cross-talk between atrial natriuretic peptide and nitric oxide receptors. Mol Cell Biochem 338, 183–189 (2010). https://doi.org/10.1007/s11010-009-0352-6

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  • DOI: https://doi.org/10.1007/s11010-009-0352-6

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