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Sieck, Gary

0000-0003-3040-9424

Mayo Clinic

Department of Physiology and Biomedical Engineering, Mayo Clinic, Rochester, Minnesota, United States.

Citations 122

Aging affects the number and morphological heterogeneity of rat phrenic motor neurons and phrenic motor axons

Physiological Reports | January 25, 2023 | Volume: 11 | Issue: 2 | Pages: No page available

10.14814/phy2.15587 | PMID 36695744

Abstract Diaphragm muscle (DIAm) motor units comprise a phrenic motor neuron (PhMN), the phrenic nerve and the muscle fibers innervated, with the size of PhMNs and axons characteristic of motor unit type. Smaller PhMNs and their axons comprise slow (type S) and fatigue‐resistant (type FR) DIAm motor units, while larger PhMNs and their axons comprise more fatigable (type FF) motor units. With aging, we have shown a loss of larger PhMNs, consistent with selective atrophy of type IIx/IIb DIAm fibers and reduced maximum DIAm force. In the present study, we hypothesized that with aging there is a loss of larger myelinated phrenic α motor axons. Female and male young (6 months) and old (24 months) Fischer 344 rats were studied. PhMNs were retrogradely labeled by intrapleural injection of 488‐conjugated CTB. The phrenic nerves were excised ~1 cm from the DIAm insertion and mounted in resin, and phrenic α motor axons were delineated based on size (i.e., >4 μm diameters). In older rats, the number of larger PhMNs and larger phrenic α motor axons were reduced. There were no differences in non‐α axons. In addition, there was evidence of demyelination of larger phrenic α motor axons in older rats. Together, these findings are consistent with the selective age‐related vulnerability of larger PhMNs and denervation of type FF motor units, which may underlie DIAm sarcopenia.
Effects of arginase inhibition on myocardial Ca2+ and contractile responses

Physiological Reports | July 22, 2022 | Volume: 10 | Issue: 14 | Pages: No page available

10.14814/phy2.15396 | PMID 35866269

AbstractNitric oxide (NO) is thought to increase cardiac contractility by increasing cytosolic Ca2+ concentration ([Ca2+]cyt) during excitation. Alternatively, NO could increase the sensitivity of the contractile response to [Ca2+]cyt (Ca2+ sensitivity). Arginase regulates NO production by competing with NO synthase (NOS), and thus, arginase inhibition should increase cardiac contractility by increasing NO production. We hypothesized that arginase inhibition increases cardiac contractility by increasing both [Ca2+]cyt and Ca2+ sensitivity. [Ca2+]cyt and contractile (sarcomere length [SL] shortening) responses to electrical stimulation were measured simultaneously in isolated rat cardiomyocytes using an IonOptix system. In the same cardiomyocytes, measurements were obtained at baseline, following 3‐min exposure to an arginase inhibitor (S‐[2‐boronoethyl]‐l‐cysteine; BEC) and following 3‐min exposure to BEC plus a NOS inhibitor (NG‐nitro‐l‐arginine‐methyl ester; l‐NAME). These responses were compared to time‐matched control cardiomyocytes that were untreated. Compared to baseline, BEC increased the amplitude and the total amount of evoked [Ca2+]cyt, and the extent and velocity of SL shortening in cardiomyocytes, whereas addition of l‐NAME mitigated these effects. The [Ca2+]cyt at 50% contraction and relaxation were not different across treatment groups indicating no effect of BEC on Ca2+ sensitivity. The [Ca2+]cyt and SL shortening responses in time‐matched controls did not vary with time. Arginase inhibition by BEC significantly increased the amplitude and the total amount of evoked [Ca2+]cyt, and the extent and velocity of SL shortening in cardiomyocytes, but did not affect Ca2+ sensitivity. These effects of BEC were mitigated by l‐NAME. Together, these results indicate an effect of NO on [Ca2+]cyt responses that then increase the contractile response of cardiomyocytes.
Mitochondrial adaptations to inactivity in diaphragm muscle fibers

Journal of Applied Physiology | June 9, 2022 | Volume: 133 | Issue: 1 | Pages: 191-204

10.1152/japplphysiol.00090.2022 | PMID 35678745

Two weeks of diaphragm (DIAm) inactivity imposed by C2SH caused reduced mitochondrial volume density, mitochondrial fragmentation, and a concomitant reduction of SDH max in type I and IIa DIAm fibers on the lesioned side. Type I and IIa DIAm fibers were far more sensitive to inactivation than type IIx/IIb fibers, which exhibited little pathology. Our results indicate that mitochondria in DIAm fibers are plastic in response to varying levels of activity.
Primary cilia in satellite cells are the mechanical sensors for muscle hypertrophy

Proceedings of the National Academy of Sciences | June 7, 2022 | Volume: 119 | Issue: 24 | Pages: No page available

10.1073/pnas.2103615119 | PMID 35671424

Skeletal muscle atrophy is commonly associated with aging, immobilization, muscle unloading, and congenital myopathies. Generation of mature muscle cells from skeletal muscle satellite cells (SCs) is pivotal in repairing muscle tissue. Exercise therapy promotes muscle hypertrophy and strength. Primary cilium is implicated as the mechanical sensor in some mammalian cells, but its role in skeletal muscle cells remains vague. To determine mechanical sensors for exercise-induced muscle hypertrophy, we established three SC-specific cilium dysfunctional mouse models— Myogenic factor 5 ( Myf5 ) -Arf-like Protein 3 ( Arl3 ) −/− , Paired box protein Pax-7 ( Pax7 )- Intraflagellar transport protein 88 homolog ( Ift88 ) −/− , and Pax7-Arl3 −/− —by specifically deleting a ciliary protein ARL3 in MYF5-expressing SCs, or IFT88 in PAX7-expressing SCs, or ARL3 in PAX7-expressing SCs, respectively. We show that the Myf5-Arl3 −/− mice develop grossly the same as WT mice. Intriguingly, mechanical stimulation-induced muscle hypertrophy or myoblast differentiation is abrogated in Myf5-Arl3 −/− and Pax7-Arl3 −/− mice or primary isolated Myf5-Arl3 −/− and Pax7-Ift88 −/− myoblasts, likely due to defective cilia-mediated Hedgehog (Hh) signaling. Collectively, we demonstrate SC cilia serve as mechanical sensors and promote exercise-induced muscle hypertrophy via Hh signaling pathway.
Diaphragm muscle function in a mouse model of early-onset spasticity

Journal of Applied Physiology | May 19, 2022 | Volume: 133 | Issue: 1 | Pages: 60-68

10.1152/japplphysiol.00157.2022 | PMID 35608200

Developmental motor control dysfunctions, including spastic cerebral palsy (sCP) often have respiratory components. Spa mutant mice exhibit a spastic phenotype closely resembling sCP symptoms. Using the spa mouse model of spastic cerebral palsy (sCP), we quantified transdiaphragmatic pressure deficits, diaphragm muscle weakness, and fiber type-specific atrophy, improving our understanding of respiratory dysfunctions in sCP.
Physiological Impact of Hypothermia: The Good, the Bad, and the Ugly

Physiology | October 11, 2021 | Volume: 37 | Issue: 2 | Pages: 69-87

10.1152/physiol.00025.2021 | PMID 34632808

Hypothermia is defined as a core body temperature of <35°C, and as body temperature is reduced the impact on physiological processes can be beneficial or detrimental. The beneficial effect of hypothermia enables circulation of cooled experimental animals to be interrupted for 1–2 h without creating harmful effects, while tolerance of circulation arrest in normothermia is between 4 and 5 min. This striking difference has attracted so many investigators, experimental as well as clinical, to this field, and this discovery was fundamental for introducing therapeutic hypothermia in modern clinical medicine in the 1950s. Together with the introduction of cardiopulmonary bypass, therapeutic hypothermia has been the cornerstone in the development of modern cardiac surgery. Therapeutic hypothermia also has an undisputed role as a protective agent in organ transplantation and as a therapeutic adjuvant for cerebral protection in neonatal encephalopathy. However, the introduction of therapeutic hypothermia for organ protection during neurosurgical procedures or as a scavenger after brain and spinal trauma has been less successful. In general, the best neuroprotection seems to be obtained by avoiding hyperthermia in injured patients. Accidental hypothermia occurs when endogenous temperature control mechanisms are incapable of maintaining core body temperature within physiologic limits and core temperature becomes dependent on ambient temperature. During hypothermia spontaneous circulation is considerably reduced and with deep and/or prolonged cooling, circulatory failure may occur, which may limit safe survival of the cooled patient. Challenges that limit safe rewarming of accidental hypothermia patients include cardiac arrhythmias, uncontrolled bleeding, and “rewarming shock.”
Tongue muscle contractile, fatigue, and fiber type properties in rats

Journal of Applied Physiology | July 29, 2021 | Volume: 131 | Issue: 3 | Pages: 1043-1055

10.1152/japplphysiol.00329.2021 | PMID 34323593

For the individual tongue muscles, relatively little quantification of uniaxial force, fatigue, and fiber type-specific properties has been documented. Here, we assessed uniaxial-specific force generation, fatigability, and muscle fiber type-specific properties in the superior and inferior longitudinal muscles, the transversalis, and the genioglossus in Fischer 344 rats. The longitudinal muscles produced the greatest isometric tetanic-specific forces. The genioglossus was more fatigue resistant and comprised higher proportions of I and IIa fibers.
Maintaining intravenous volume mitigates hypothermia‐induced myocardial dysfunction and accumulation of intracellular Ca2+

Experimental Physiology | March 17, 2021 | Volume: 106 | Issue: 5 | Pages: 1196-1207

10.1113/ep089397 | PMID 33728692

New Findings What is the central question of this study? Detailed guidelines for volume replacement to counteract hypothermia‐induced intravascular fluid loss are lacking. Evidence suggests colloids might have beneficial effects compared to crystalloids. Are central haemodynamic function and level of hypothermia‐induced calcium overload, as a marker of cardiac injury, restored by fluid substitution during rewarming, and are colloids favourable to crystalloids? What is the main finding and its importance? Infusion with crystalloid or dextran during rewarming abolished post‐hypothermic cardiac dysfunction, and partially mitigated myocardial calcium overload. The effects of volume replacement to support haemodynamic function are comparable to those using potent cardio‐active drugs. These findings underline the importance of applying intravascular volume replacement to maintain euvolaemia during rewarming. AbstractPrevious research exploring pathophysiological mechanisms underlying circulatory collapse after rewarming victims of severe accidental hypothermia has documented post‐hypothermic cardiac dysfunction and hypothermia‐induced elevation of intracellular Ca2+ concentration ([Ca2+]i) in myocardial cells. The aim of the present study was to examine if maintaining euvolaemia during rewarming mitigates cardiac dysfunction and/or normalizes elevated myocardial [Ca2+]i. A total of 21 male Wistar rats (300 g) were surface cooled to 15°C, then maintained at 15°C for 4 h, and subsequently rewarmed to 37°C. The rats were randomly assigned to one of three groups: (1) non‐intervention control (n = 7), (2) dextran treated (i.v. 12 ml/kg dextran 70; n = 7), or (3) crystalloid treated (24 ml/kg 0.9% i.v. saline; n = 7). Infusions occurred during the first 30 min of rewarming. Arterial blood pressure, stroke volume (SV), cardiac output (CO), contractility (dP/dtmax) and blood gas changes were measured. Post‐hypothermic changes in [Ca2+]i were measured using the method of radiolabelled Ca2+ (45Ca2+). Untreated controls displayed post‐hypothermic cardiac dysfunction with significantly reduced CO, SV and dP/dtmax. In contrast, rats receiving crystalloid or dextran treatment showed a return to pre‐hypothermic control levels of CO and SV after rewarming, with the dextran group displaying significantly better amelioration of post‐hypothermic cardiac dysfunction than the crystalloid group. Compared to the post‐hypothermic increase in myocardial [Ca2+]i in non‐treated controls, [Ca2+]i values with crystalloid and dextran did not increase to the same extent after rewarming. Volume replacement with crystalloid or dextran during rewarming abolishes post‐hypothermic cardiac dysfunction, and partially mitigates the hypothermia‐induced elevation of [Ca2+]i.
Improving gas exchange and exercise tolerance in mild COPD patients

The Journal of Physiology | February 12, 2021 | Volume: 599 | Issue: 7 | Pages: 1943-1944

10.1113/jp281323 | PMID 33576012

Growth and survival characteristics of spa mice

Animal Models and Experimental Medicine | October 10, 2020 | Volume: 3 | Issue: 4 | Pages: 319-324

10.1002/ame2.12137 | PMID 33532707

AbstractCharacterization of growth and survival of mice displaying early onset hypertonic symptoms is critical as these animals are important for research investigating mechanisms and treatments of pediatric conditions associated with hypertonia, such as cerebral palsy. Currently, most animal models of cerebral palsy reproduce risk factors for developing this condition, with most failing to develop the physical symptoms or failing to survive in the postnatal period. The B6.Cg‐Glrbspa/J (Gly receptor mutation) transgenic mouse (spa mouse), displays symptoms of early onset hypertonia, though little has been reported on growth and survival, with no reports of growth and survival since genotyping became available. We found that the majority of spa mice display symptoms by P14‐P16. Of mice surviving to weaning, only ~9% were spa mice. By weaning age, spa mice had significantly lower weights than their heterozygote and wild‐type littermates. Of mice that died after weaning and prior to use in experiments or being culled, 48% were spa mice. The poor growth and decreased survival of spa mice across multiple developmental and adult ages resembled the varied survival rates observed in humans with mild or severe cerebral palsy. The understanding of the expected survival of these mice is helpful for planning breeding and animal numbers for experiments. Due to the symptoms and timing of symptom onset, spa mice will be valuable in uncovering mechanisms and long‐term effects of early onset hypertonia in order to move toward interventions for these conditions.