Comprehensive Physiology Wiley Online Library

The Growth Hormone Secretory Pattern and Statural Growth

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 How is the Growth Hormone Secretory Pattern Analyzed?
1.1 General Considerations in Pulse Analysis of Growth Hormone Secretion
1.2 Construction of Data Arrays or Hormone Profiles
1.3 Sampling Interval and Aliasing
1.4 Duration of Sampling
1.5 Discrete or Integrated Samples
1.6 Assays and Noise
1.7 Basic Evaluation
1.8 Stationarization
1.9 Analysis of Profiles
1.10 Time Series Analysis
1.11 Deconvolution Analysis
1.12 Baseline Occupancy
1.13 Chaos
1.14 Neural Networks
2 Characterization of Growth Hormone Secretory Patterns
2.1 Ontogeny of Episodic Growth Hormone Secretion
2.2 Growth Hormone Secretory Patterns in the Prepubertal Period
2.3 Puberty and Effects of Gonadal Steroids on the Growth Hormone Secretory Pattern
2.4 Growth Hormone Secretory Patterns in Adulthood
2.5 Other Endocrine Inputs Affecting Growth Hormone Secretory Patterns
2.6 Extrinsic Factors Affecting Growth Hormone Pulsatility
3 How Does the Growth Hormone Secretory Pattern Reflect the Episodic Nature of Hypothalamic Control Mechanisms?
3.1 Growth Hormone–Releasing Hormone and Somatostatin Interactions Generate Growth Hormone Pulsatility
3.2 Other Growth Hormone Secretogogues
3.3 Growth Hormone Feedback Effects on Endogenous Growth Hormone Pulsatility
4 How is The Growth Hormone Secretory Signal Modified in its Passage from the Pituitary to the Peripheral Target Tissues?
4.1 How Are Growth Hormone Patterns Modified by Interactions with Growth Hormone Binding Proteins?
5 How are the Temporal Elements of the Growth Hormone Signal Detected and Interpreted by the Target Tissues?
5.1 Pattern‐Dependent Growth Hormone Responses
5.2 Growth Hormone Patterns and Insulin‐Like Growth Factor I Generation
6 What is the Significance of the Growth Hormone Secretory Pattern for Statural Growth?
6.1 Animal Studies
6.2 Human Studies
6.3 Indirect Manipulation of Growth Hormone Secretory Pattern
7 Summary
Figure 1. Figure 1.

Growth hormone (GH) secretion is highly episodic in the rat and human. A: The regular ultradian rhythm of GH secretion in the conscious male rat first described by Tannenbaum and Martin , and shown here by serial blood microsampling for 48 h across two light/dark periods . B:A 24 h serum GH concentration profile from an 8‐year‐old boy with a peak GH response to an insulin tolerance test (ITT). Note the pulsatile GH secretion with a dominant periodicity of 3 h, and the resemblance between the GH profile and the test (the ITT) of GH reserve.

Figure 2. Figure 2.

Aliasing can markedly alter the conclusions drawn from (a) sampling a true oscillatory cycle, (b) the effect of irregular sampling, and (c and d) the effect of regular sampling with time intervals unsuitable for the cycle period under study.

Figure 3. Figure 3.

Effect of sampling every 2.5 min (upper panel) or every 20 min (lower panel) on the shape of a growth hormone profile obtained from a patient after subcutaneous growth hormone–releasing hormone (GHRH[1–29]NH2) administration.

Figure 4. Figure 4.

Continuous venous sampling can be achieved in children without obvious restraint or stress! [Photograph kindly supplied by Dr. K. Albertsson Wikland.]

Figure 5. Figure 5.

The application of the technique of autocorrelation to a 24 h serum growth hormone concentration profile. Upper panel, serum profile; lower panel, autocorrelation function with a significant lag time of 240 mins (P < 0.05). This can be checked by determining the periodicity of pulses in the raw data.

Figure 6. Figure 6.

Fourier transformation to a 24‐h serum growth hormone (GH) concentration profile. The upper panel shows the spectral power of the GH profile shown in the lower panel, illustrating a dominant period of 240 mins with subharmonics at 120 and 480 mins.

Figure 7. Figure 7.

Highly pulsatile growth hormone (GH) secretion appears above a raised baseline level in premature infants. The figure shows a GH profile from a 34‐wk premature infant obtained by automated blood microsampling within 24 h of delivery.

From Adcock et al.
Figure 8. Figure 8.

The asymptotic relationship between growth hormone secretion and growth rate in children expressed as a standard deviation score (Z score).

Figure 9. Figure 9.

Changes in mean 24‐h growth hormone secretion rate through the stages of pubertal development. Closed circles, girls; closed squares, boys.

From Albertsson et al.
Figure 10. Figure 10.

Growth hormone secretory profiles obtained from conscious male and female rats, either intact (a,f), subjected to gonadal suppression by a long acting gonadotropin‐releasing hormone analog (triptorelin) (b,e), or gonadectomized prepubertally (c,d).

From E. Gevers, J. M Wit, and I. C. A. F. Robinson (unpublished)
Figure 11. Figure 11.

Individual 24 h serum growth hormone concentration profiles at different ages throughout the human lifespan.

Figure 12. Figure 12.

Plasma growth hormone (GH) profile across the estrus cycle in a single female rat sampled every 12 min for 5 days. Note the high basal GH level and increased rapid pulsatility during dark periods, particularly around proestrus, as indicated by the rise in PRL (arrow), which was also measured in some extra samples taken on each afternoon.

From Clark et al.
Figure 13. Figure 13.

Pulsatile growth hormone secretion is suppressed in untreated diabetic male rats, but returns rapidly once they are treated with insulin for 2 or 7 days.

From
Figure 14. Figure 14.

Growth hormone–releasing hormone (GRF) is secreted in frequent pulses, only some of which are associated with episodes of growth hormone (GH) secretion. Pituitary responsiveness depends on the prevailing somatostatin (SRIF) tone. If it is intermittent, it would give rise to the episodic GH pattern typical of male rats (left), whereas a more stable somatostatin tone would generate a more continuous irregular pattern typical of female rats (right).

From Robinson
Figure 15. Figure 15.

Continuous exposure to growth hormone–releasing hormone (GRF) amplifies growth hormone secretory episodes in conscious male rats, but the pattern still remains highly pulsatile . [Data from Robinson and Clark .]

Figure 16. Figure 16.

Somatostatin (SRIF) infusion suppresses growth hormone (GH) secretion, but if the infusion is interrupted every 3 h, a series of rebound GH secretory bursts can be elicited, mimicking the male pattern. If this is continued, it stimulates growth in normal female rats . [Data from Wells et al. .]

Figure 17. Figure 17.

The role of growth hormone–releasing hormone (GHRH) and somatostatin in the generation of growth hormone (GH) pulses in man. a: 3‐hourly saline infusions with bolus injections of saline, b: 3‐hourly saline infusions with bolus injections of GHRH NH2. c: 3‐hourly intermittent somatostatin (SS 1–14) infusions with bolus injections of saline, d: 3‐hourly somatostatin (SS 1–14) infusions with bolus injections of GHRH NH2. Infusions are shown by boxed areas and injections by the arrows. [From Hindmarsh et al. .]

Figure 18. Figure 18.

Regular 3 hourly pulses of exogenous growth hormone (GH) (arrows) will entrain endogenous episodic GH secretion in conscious male rats.

From Carlsson and Jansson
Figure 19. Figure 19.

Different signals are obtained with a mixed pattern of continuous (c) and pulsatile (p) intravenous growth hormone (GH) infusions in GH‐deficient dwarf rats. A: Growth promotion increases with the pulsatile component of a mixed infusion pattern, whereas B: hepatic GH receptor binding (top) and the circulating level of growth hormone binding protein (GHBP) (bottom) increase with the continuous component of the infusions.

From Gevers et al.
Figure 20. Figure 20.

The expression of many hepatic genes, such as CYP2C11 or CYP2C12, is regulated by the sexually dimorphic growth hormone (GH) secretory pattern, even in severely GH‐deficient dwarf rats. Continuous intravenous infusions of GH in male dwarf rats ‘feminize’ the pattern of expression of these genes (suppressing 2C11, open bars, while inducing 2C12, solid bars) at doses below those necessary to induce growth or alter insulin‐like growth factor I expression (hatched bars).

From Wells et al.
Figure 21. Figure 21.

Serum insulin‐like growth factor I (IGF‐I) and serum growth hormone binding protein (GHBP) levels are more sensitive to growth hormone (GH) infused continuously (solid bars) than when it is given by daily injection (open bars) to hypophysectomized female rats. Hatched bars indicate vehicle‐infused rats.

From Clark et al.
Figure 22. Figure 22.

Growth in hypophysectomized rats receiving growth hormone (GH) by intravenous infusion is both dose‐ and pattern‐dependent. Rats given intravenous pulses of GH every 3 h to mimic the male pattern grow faster than rats given the same dose by continuous infusion.

From Clark et al.
Figure 23. Figure 23.

Intermittent (triangles) and pulsatile (squares) growth hormone replacement in hypophysectomized female rats generate nonparallel dose‐response curves for body weight gain (left panel) but not for bone growth, as assessed by epiphyseal tibial width (right panel).

From Clark et al.
Figure 24. Figure 24.

a: Body weight change, b: tibial epiphyseal width, c: ovarian weight, and d: retroperitoneal fat pad weight in dwarf growth hormone‐deficient female rats with dietary‐induced obesity that were treated with human growth hormone (hGH) by infusion or single daily injections. These treatments caused diametrically opposite effects on weight gain, and differential effects on fat despite equivalent effects on skeletal growth.

From Clark et al.
Figure 25. Figure 25.

Growth of a boy with growth hormone deficiency (peak growth hormone response to insulin‐induced hypoglycemia was 6.3 mU/L; the normal response is > 13.5 mU/L) shown by the dashed line and compared to the 50th height centile for the normal population (continuous line). Note that the child grew along the 50th height centile until 1 year of age; thereafter growth failed. Growth‐hormone therapy (initiated at arrow) was associated with rapid growth until the 50th height centile was reached, when growth rate returned to normal.

Figure 26. Figure 26.

Growth response (expressed as height velocity standard deviation score; [HV SDS]) to different doses of growth hormone treatment in two groups of children with different pretreatment height velocities.

Figure 27. Figure 27.

Growth response (change in height velocity expressed as a standard deviation score) over 1 year using a similar weekly dose of growth hormone but given as either left: four units thrice weekly, middle: two units 6 days per week, or right: one unit twice daily for 6 days per week.

From Smith et al.
Figure 28. Figure 28.

Effects of intravenous infusions of saline (S), continuous growth hormone–releasing hormone (GHRH) (C), or pulsatile GHRH (P) given to (a) normal female rats or (b) male rats given monosodium glutamate (MSG) neonatally to destroy GHRH cells. At this dose level (8 μg/day), only pulsatile GHRH exposure stimulated growth significantly.

From Clark and Robinson
Figure 29. Figure 29.

This figure shows the relationship between the amount of growth hormone secreted in 24 h and the growth rate observed in a group of children receiving growth hormone–releasing hormone NH2 by continuous subcutaneous infusion over a 1 yr period.

From Brain et al.
Figure 30. Figure 30.

The effects of growth hormone (GH) secretagogues on growth in rats are highly dependent on their pattern of administration. The initial response to continuous infusion of the GH secretagogue, G7039 (circles), was greater than in rats given vehicle alone (squares) but faded rapidly when compared with a group given the same dose of G7039 by twice daily injections (triangles) [Data from McDowell et al. .]



Figure 1.

Growth hormone (GH) secretion is highly episodic in the rat and human. A: The regular ultradian rhythm of GH secretion in the conscious male rat first described by Tannenbaum and Martin , and shown here by serial blood microsampling for 48 h across two light/dark periods . B:A 24 h serum GH concentration profile from an 8‐year‐old boy with a peak GH response to an insulin tolerance test (ITT). Note the pulsatile GH secretion with a dominant periodicity of 3 h, and the resemblance between the GH profile and the test (the ITT) of GH reserve.



Figure 2.

Aliasing can markedly alter the conclusions drawn from (a) sampling a true oscillatory cycle, (b) the effect of irregular sampling, and (c and d) the effect of regular sampling with time intervals unsuitable for the cycle period under study.



Figure 3.

Effect of sampling every 2.5 min (upper panel) or every 20 min (lower panel) on the shape of a growth hormone profile obtained from a patient after subcutaneous growth hormone–releasing hormone (GHRH[1–29]NH2) administration.



Figure 4.

Continuous venous sampling can be achieved in children without obvious restraint or stress! [Photograph kindly supplied by Dr. K. Albertsson Wikland.]



Figure 5.

The application of the technique of autocorrelation to a 24 h serum growth hormone concentration profile. Upper panel, serum profile; lower panel, autocorrelation function with a significant lag time of 240 mins (P < 0.05). This can be checked by determining the periodicity of pulses in the raw data.



Figure 6.

Fourier transformation to a 24‐h serum growth hormone (GH) concentration profile. The upper panel shows the spectral power of the GH profile shown in the lower panel, illustrating a dominant period of 240 mins with subharmonics at 120 and 480 mins.



Figure 7.

Highly pulsatile growth hormone (GH) secretion appears above a raised baseline level in premature infants. The figure shows a GH profile from a 34‐wk premature infant obtained by automated blood microsampling within 24 h of delivery.

From Adcock et al.


Figure 8.

The asymptotic relationship between growth hormone secretion and growth rate in children expressed as a standard deviation score (Z score).



Figure 9.

Changes in mean 24‐h growth hormone secretion rate through the stages of pubertal development. Closed circles, girls; closed squares, boys.

From Albertsson et al.


Figure 10.

Growth hormone secretory profiles obtained from conscious male and female rats, either intact (a,f), subjected to gonadal suppression by a long acting gonadotropin‐releasing hormone analog (triptorelin) (b,e), or gonadectomized prepubertally (c,d).

From E. Gevers, J. M Wit, and I. C. A. F. Robinson (unpublished)


Figure 11.

Individual 24 h serum growth hormone concentration profiles at different ages throughout the human lifespan.



Figure 12.

Plasma growth hormone (GH) profile across the estrus cycle in a single female rat sampled every 12 min for 5 days. Note the high basal GH level and increased rapid pulsatility during dark periods, particularly around proestrus, as indicated by the rise in PRL (arrow), which was also measured in some extra samples taken on each afternoon.

From Clark et al.


Figure 13.

Pulsatile growth hormone secretion is suppressed in untreated diabetic male rats, but returns rapidly once they are treated with insulin for 2 or 7 days.

From


Figure 14.

Growth hormone–releasing hormone (GRF) is secreted in frequent pulses, only some of which are associated with episodes of growth hormone (GH) secretion. Pituitary responsiveness depends on the prevailing somatostatin (SRIF) tone. If it is intermittent, it would give rise to the episodic GH pattern typical of male rats (left), whereas a more stable somatostatin tone would generate a more continuous irregular pattern typical of female rats (right).

From Robinson


Figure 15.

Continuous exposure to growth hormone–releasing hormone (GRF) amplifies growth hormone secretory episodes in conscious male rats, but the pattern still remains highly pulsatile . [Data from Robinson and Clark .]



Figure 16.

Somatostatin (SRIF) infusion suppresses growth hormone (GH) secretion, but if the infusion is interrupted every 3 h, a series of rebound GH secretory bursts can be elicited, mimicking the male pattern. If this is continued, it stimulates growth in normal female rats . [Data from Wells et al. .]



Figure 17.

The role of growth hormone–releasing hormone (GHRH) and somatostatin in the generation of growth hormone (GH) pulses in man. a: 3‐hourly saline infusions with bolus injections of saline, b: 3‐hourly saline infusions with bolus injections of GHRH NH2. c: 3‐hourly intermittent somatostatin (SS 1–14) infusions with bolus injections of saline, d: 3‐hourly somatostatin (SS 1–14) infusions with bolus injections of GHRH NH2. Infusions are shown by boxed areas and injections by the arrows. [From Hindmarsh et al. .]



Figure 18.

Regular 3 hourly pulses of exogenous growth hormone (GH) (arrows) will entrain endogenous episodic GH secretion in conscious male rats.

From Carlsson and Jansson


Figure 19.

Different signals are obtained with a mixed pattern of continuous (c) and pulsatile (p) intravenous growth hormone (GH) infusions in GH‐deficient dwarf rats. A: Growth promotion increases with the pulsatile component of a mixed infusion pattern, whereas B: hepatic GH receptor binding (top) and the circulating level of growth hormone binding protein (GHBP) (bottom) increase with the continuous component of the infusions.

From Gevers et al.


Figure 20.

The expression of many hepatic genes, such as CYP2C11 or CYP2C12, is regulated by the sexually dimorphic growth hormone (GH) secretory pattern, even in severely GH‐deficient dwarf rats. Continuous intravenous infusions of GH in male dwarf rats ‘feminize’ the pattern of expression of these genes (suppressing 2C11, open bars, while inducing 2C12, solid bars) at doses below those necessary to induce growth or alter insulin‐like growth factor I expression (hatched bars).

From Wells et al.


Figure 21.

Serum insulin‐like growth factor I (IGF‐I) and serum growth hormone binding protein (GHBP) levels are more sensitive to growth hormone (GH) infused continuously (solid bars) than when it is given by daily injection (open bars) to hypophysectomized female rats. Hatched bars indicate vehicle‐infused rats.

From Clark et al.


Figure 22.

Growth in hypophysectomized rats receiving growth hormone (GH) by intravenous infusion is both dose‐ and pattern‐dependent. Rats given intravenous pulses of GH every 3 h to mimic the male pattern grow faster than rats given the same dose by continuous infusion.

From Clark et al.


Figure 23.

Intermittent (triangles) and pulsatile (squares) growth hormone replacement in hypophysectomized female rats generate nonparallel dose‐response curves for body weight gain (left panel) but not for bone growth, as assessed by epiphyseal tibial width (right panel).

From Clark et al.


Figure 24.

a: Body weight change, b: tibial epiphyseal width, c: ovarian weight, and d: retroperitoneal fat pad weight in dwarf growth hormone‐deficient female rats with dietary‐induced obesity that were treated with human growth hormone (hGH) by infusion or single daily injections. These treatments caused diametrically opposite effects on weight gain, and differential effects on fat despite equivalent effects on skeletal growth.

From Clark et al.


Figure 25.

Growth of a boy with growth hormone deficiency (peak growth hormone response to insulin‐induced hypoglycemia was 6.3 mU/L; the normal response is > 13.5 mU/L) shown by the dashed line and compared to the 50th height centile for the normal population (continuous line). Note that the child grew along the 50th height centile until 1 year of age; thereafter growth failed. Growth‐hormone therapy (initiated at arrow) was associated with rapid growth until the 50th height centile was reached, when growth rate returned to normal.



Figure 26.

Growth response (expressed as height velocity standard deviation score; [HV SDS]) to different doses of growth hormone treatment in two groups of children with different pretreatment height velocities.



Figure 27.

Growth response (change in height velocity expressed as a standard deviation score) over 1 year using a similar weekly dose of growth hormone but given as either left: four units thrice weekly, middle: two units 6 days per week, or right: one unit twice daily for 6 days per week.

From Smith et al.


Figure 28.

Effects of intravenous infusions of saline (S), continuous growth hormone–releasing hormone (GHRH) (C), or pulsatile GHRH (P) given to (a) normal female rats or (b) male rats given monosodium glutamate (MSG) neonatally to destroy GHRH cells. At this dose level (8 μg/day), only pulsatile GHRH exposure stimulated growth significantly.

From Clark and Robinson


Figure 29.

This figure shows the relationship between the amount of growth hormone secreted in 24 h and the growth rate observed in a group of children receiving growth hormone–releasing hormone NH2 by continuous subcutaneous infusion over a 1 yr period.

From Brain et al.


Figure 30.

The effects of growth hormone (GH) secretagogues on growth in rats are highly dependent on their pattern of administration. The initial response to continuous infusion of the GH secretagogue, G7039 (circles), was greater than in rats given vehicle alone (squares) but faded rapidly when compared with a group given the same dose of G7039 by twice daily injections (triangles) [Data from McDowell et al. .]

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Iain C. A. F. Robinson, Peter C. Hindmarsh. The Growth Hormone Secretory Pattern and Statural Growth. Compr Physiol 2011, Supplement 24: Handbook of Physiology, The Endocrine System, Hormonal Control of Growth: 329-395. First published in print 1999. doi: 10.1002/cphy.cp070512